Intercellular adhesion molecules (ICAMs) and spermatogenesis

Human Reproduction Update

Volumn 19, Issue 2, 2013, Pages 167-186

  Xiao, Xiang ^a   Murk, Dolores D ^a   Cheng, C Yan ^a  

^a POPULATION COUNCIL   (United States)

Author keywords

Blood testis barrier; Ectoplasmic specialization; ICAM; Spermatogenesis; Testis

Indexed keywords

GLYCOPROTEIN; INTERCELLULAR ADHESION MOLECULE 1; INTERCELLULAR ADHESION MOLECULE 2; INTERCELLULAR ADHESION MOLECULE 3; INTERCELLULAR ADHESION MOLECULE 4; INTERCELLULAR ADHESION MOLECULE 5; UNCLASSIFIED DRUG;

BLOOD TESTIS BARRIER; CELL ADHESION; CELL MOTILITY; HUMAN; PRIORITY JOURNAL; REVIEW; SERTOLI CELL; SPERMATID; SPERMATOGENESIS; SYSTEMATIC REVIEW;

BLOOD-TESTIS BARRIER; CELL ADHESION MOLECULES; EPITHELIUM; HUMANS; MALE; SEMINIFEROUS EPITHELIUM; SERTOLI CELLS; SPERMATIDS; SPERMATOGENESIS; SPERMATOZOA; TESTIS; TIGHT JUNCTIONS;

EID: 84874499109     PISSN: 13554786     EISSN: 14602369     Source Type: Journal    
DOI: 10.1093/humupd/dms049     Document Type: Review

References (267)

1. Adamson P, Etienne S, Couraud PO, Calder V, Greenwood J. Lymphocyte migration through brain endothelial cell monolayers involves signaling through endothelial ICAM-1 via a rho-dependent pathway. J Immunol 1999;162:2964-2973.
2. Alcaide P, Martinelli R, Newton G, Williams MR, Adam A, Vincent PA, Luscinskas FW. p120-Catenin prevents neutrophil transmigration independently of RhoA inhibition by impairing Src dependent VE-cadherin phosphorylation. Am J Physiol Cell Physiol 2012;303:C385-C395.
3. Allingham MJ, van Buul JD, Burridge K. ICAM-1-mediated, Src- and Pyk2-dependent vascular endothelial cadherin tyrosine phosphorylation is required for leukocyte transendothelial migration. J Immunol 2007;179:4053-4064.
4. Allport JR, Muller WA, Luscinskas FW. Monocytes induce reversible focal changes in vascular endothelial cadherin complex during transendothelial migration under flow. J Cell Biol 2000;148:203-216.
5. Amann RP. The cycle of the seminiferous epithelium in humans: a need to revisit? J Androl 2008;29:469-487.
6. Amos C, Romero IA, Schultze C, Rousell J, Pearson JD, Greenwood J, Adamson P. Cross-linking of brain endothelial intercellular adhesion molecule (ICAM)-1 induces association of ICAM-1 with detergent-insoluble cytoskeletal fraction. Arterioscler Thromb Vasc Biol 2001;21:810-816.
7. Annaert WG, Esselens C, Baert V, Boeve C, Snellings G, Cupers P, Craessaerts K, De Strooper B. Interaction with telencephalin and the amyloid precursor protein predicts a ring structure for presenilins. Neuron 2001;32:579-589.
8. Aricescu AR, Jones EY. Immunoglobulin superfamily cell adhesion molecules: zippers and signals. Curr Opin Cell Biol 2007;19:543-550.
9. Barreiro O, Yanez-Mo M, Serrador JM, Montoya MC, Vicente-Manzanares M, Tejedor R, Furthmayr H, Sanchez-Madrid F. Dynamic interaction of VCAM-1 and ICAM-1 with moesin and ezrin in a novel endothelial docking structure for adherent leukocytes. J Cell Biol 2002;157:1233-1245.
10. Barreiro O, Zamai M, Yanez-Mo M, Tejera E, Lopez-Romero P, Monk PN, Gratton E, Caiolfa VR, Sanchez-Madrid F. Endothelial adhesion receptors are recruited to adherent leukocytes by inclusion in preformed tetraspanin nanoplatforms. J Cell Biol 2008;183:527-542.
11. Berney SM, Schaan T, Alexander JS, Peterman G, Hoffman PA, Wolf RE, van der Heyde H, Atkinson TP. ICAM-3 (CD50) cross-linking augments signaling in CD3-activated peripheral human T lymphocytes. J Leukoc Biol 1999; 65:867-874.
12. Billig H, Furuta I, Rivier C, Tapanainen J, Parvinen M, Hsueh AJ. Apoptosis in testis germ cells: developmental changes in gonadotropin dependence and localization to selective tubule stages. Endocrinology 1995;136:5-12.
13. Bouchard MJ, Dong Y, McDermott BM Jr, Lam DH, Brown KR, Shelanski M, Bellve AR, Racaniello VR. Defects in nuclear and cytoskeletal morphology and mitochondrial localization in spermatozoa of mice lacking nectin-2, a component of cell-cell adherens junctions. Mol Cell Biol 2000;20:2865-2873.
14. Brummendorf T, Lemmon V. Immunoglobulin superfamily receptors: cis-interactions, intracellular adapters and alternative splicing regulate adhesion. Curr Opin Cell Biol 2001;13:611-618.
15. Byers S, Jegou B, MacCalman C, Blaschuk O. Sertoli cell adhesion molecules and the collective organization of the testis. In: Russell LD, Griswold MD (eds). The Sertoli Cell. Clearwater: Cache River Press, 1993a, 461-476.
16. Byers S, Pelletier RM, Suarez-Quain C. Sertoli cell junctions and the seminiferous epithelium barrier. In: Russell LD, Griswold MD (eds). The Sertoli Cell. Clearwater: Cache River Press, 1993b, 431-446.
17. Carman CV, Springer TA. A transmigratory cup in leukocyte diapedesis both through individual vascular endothelial cells and between them. J Cell Biol 2004; 167:377-388.
18. Carman CV, Jun CD, Salas A, Springer TA. Endothelial cells proactively form microvilli-like membrane projections upon intercellular adhesion molecule 1 engagement of leukocyte LFA-1. J Immunol 2003;171:6135-6144.
19. Cavallaro U, Dejana E. Adhesion molecule signalling: not always a sticky business. Nat Rev Mol Cell Biol 2011;12:189-197.
20. Cepek KL, Shaw SK, Parker CM, Russell GJ, Morrow JS, Rimm DL, Brenner MB. Adhesion between epithelial cells and T lymphocytes mediated by E-cadherin and the alpha E beta 7 integrin. Nature 1994;372:190-193.
21. Chen H, Fok KL, Yu S, Jiang J, Chen Z, Gui Y, Cai Z, Chan HC. CD147 is required for matrix metalloproteinases-2 production and germ cell migration during spermatogenesis. Mol Hum Reprod 2011;17:405-414.
22. Chen L, Bi J, Nakai M, Bunick D, Couse JF, Korach KS, Nowak RA. Expression of basigin in reproductive tissues of estrogen receptor-a or -b null mice. Reprod 2010;139:1057-1066.
23. Cheng CY, Mruk DD. Cell junction dynamics in the testis: Sertoli-germ cell interactions and male contraceptive development. Physiol Rev 2002;82:825-874.
24. Cheng CY, Mruk DD. A local autocrine axis in the testes that regulates spermatogenesis. Nat Rev Endocrinol 2010;6:380-395.
25. Cheng CY, Mruk DD. The blood-testis barrier and its implications for male contraception. Pharmacol Rev 2012;64:16-64.
26. Cheng CY, Lie PP, Mok KW, Cheng YH, Wong EW, Mannu J, Mathur PP, Yan HH, Mruk DD. Interactions of laminin beta3 fragment with beta1-integrin receptor: a revisit of the apical ectoplasmic specialization-blood-testis-barrierhemidesmosome functional axis in the testis. Spermatogenesis 2011a;1:174-185.
27. Cheng CY, Wong EW, Lie PP, Li MW, Su L, Siu ER, Yan HH, Mannu J, Mathur PP, Bonanomi M et al. Environmental toxicants and male reproductive function. Spermatogenesis 2011b;1:2-13.
28. Chui K, Trivedi A, Cheng CY, Cherbavaz DB, Dazin PF, Huynh ALT, Mitchell JB, Rabinovich GA, Noble-Haeusslein LJ, John CM. Characterization and functionality of proliferative human Sertoli cells. Cell Transplant 2011;20:619-635.
29. Clark PR, Manes TD, Pober JS, Kluger MS. Increased ICAM-1 expression causes endothelial cell leakiness, cytoskeletal reorganization and junctional alterations. J Invest Dermatol 2007;127:762-774.
30. Clermont Y. The cycle of the seminiferous epithelium in man. Am J Anat 1963; 112:35-51.
31. Clermont Y. Kinetics of spermatogenesis in mammals: seminiferous epithelium cycle and spermatogonial renewal. Physiol Rev 1972;52:198-235.
32. Conant K, Lonskaya I, Szklarczyk A, Krall C, Steiner J, Maguire-Zeiss K, Lim ST. Methamphetamine-associated cleavage of the synaptic adhesion molecule intercellular adhesion molecule-5. J Neurochem 2011;118:521-532.
33. Costantini C, Calzetti F, Perbellini O, Micheletti A, Scarponi C, Lonardi S, Pelletier M, Schakel K, Pizzolo G, Facchetti F et al. Human neutrophils interact with both 6-sulfo LacNAc+ DC and NK cells to amplify NK-derived IFN{gamma}: role of CD18, ICAM-1, and ICAM-3. Blood 2011;117:1677-1686.
34. Couty JP, Rampon C, Leveque M, Laran-Chich MP, Bourdoulous S, Greenwood J, Couraud PO. PECAM-1 engagement counteracts ICAM-1-induced signaling in brain vascular endothelial cells. J Neurochem 2007;103:793-801.
35. Cremer H, Lange R, Christoph A, Plomann M, Vopper G, Roes J, Brown R, Baldwin S, Kraemer P, Scheff S et al. Inactivation of the N-CAM gene in mice results in size reduction of the olfactory bulb and deficits in spatial learning. Nature 1994;367:455-459.
36. Cserti-Gazdewich CM, Dzik WH, Erdman L, Ssewanyana I, Dhabangi A, Musoke C, Kain KC. Combined measurement of soluble and cellular ICAM-1 among children with Plasmodium falciparum malaria in Uganda. Malar J 2010;9:233.
37. Cyr DG. Connexins and pannexins: coordinating cellular communication in the testis and epididymis. Spermatogenesis 2011;1:325-338.
38. De Cesaris P, Starace D, Riccioli A, Padula F, Filippini A, Ziparo E. Tumor necrosis factor-a induces interleukin-6 production and integrin ligand expression by distinct transduction pathways. J Biol Chem 1998;273:7566-7571.
39. De Cesaris P, Starace D, Starace G, Filippini A, Stefanini M, Ziparo E. Activation of Jun N-terminal kinase/stress-activated protein kinase pathway by tumor necrosis factor a leads to intercellular adhesion molecule-1 expression. J Biol Chem 1999; 274:28978-28982.
40. de Kretser DM, Kerr JB. The cytology of the testis. In: Knobil E, Neill JB, Ewing LL, Greenwald GS, Markert CL, Pfaff DW (eds). The Physiology of Reproduction, Vol. 1. New York: Raven Press, 1988, 837-932.
41. Dermody TS, Kirchner E, Guglielmi KM, Stehle T. Immunoglobulin superfamily virus receptors and the evolution of adaptive immunity. PLoS Pathog 2009;5:e1000481.
42. Di Lorenzo A, Manes TD, Davalos A, Wright PL, Sessa WC. Endothelial reticulon-4B (Nogo-B) regulates ICAM-1-mediated leukocyte transmigration and acute inflammation. Blood 2011;117:2284-2295.
43. Dirami G, Ravindranath N, Achi MV, Dym M. Expression of Notch pathway components in spermatogonia and Sertoli cells of neonatal mice. J Androl 2001; 22:944-952.
44. Doulet N, Donnadieu E, Laran-Chich MP, Niedergang F, Nassif X, Couraud PO, Bourdoulous S. Neisseria meningitidis infection of human endothelial cells interferes with leukocyte transmigration by preventing the formation of endothelial docking structures. J Cell Biol 2006;173:627-637.
45. Dube E, Cyr DG. The blood-epididymis barrier and human male fertility. Adv Exp Med Biol 2012;763:218-236.
46. Dym M, Cavicchia J. Junctional morphology of the testis. Biol Reprod 1978;18:1-15.
47. Dym M, Fawcett DW. The blood-testis barrier in the rat and the physiological compartmentation of the seminiferous epithelium. Biol Reprod 1970;3:308-326.
48. Elkin N, Piner J, Sharpe R. Toxicant-induced leakage of germ cell-specific proteins from seminiferous tubules in the rat: relatinship to blood-testis barrier integrity and prospects for biomonitoring. Toxicol Sci 2010;117:439-448.
49. Esselens C, Oorschot V, Baert V, Raemaekers T, Spittaels K, Serneels L, Zheng H, Saftig P, De Strooper B, Klumperman J et al. Presenilin 1 mediates the turnover of telencephalin in hippocampal neurons via an autophagic degradative pathway. J Cell Biol 2004;166:1041-1054.
50. Estecha A, Aguilera-Montilla N, Sanchez-Mateos P, Puig-Kroger A. RUNX3 regulates intercellular adhesion molecule 3 (ICAM-3) expression during macrophage differentiation and monocyte extravasation. PLoS ONE 2012;7:e33313.
51. Etienne-Manneville S, Manneville JB, Adamson P, Wilbourn B, Greenwood J, Couraud PO. ICAM-1-coupled cytoskeletal rearrangements and transendothelial lymphocyte migration involve intracellular calcium signaling in brain endothelial cell lines. J Immunol 2000;165:3375-3383.
52. Etienne S, Adamson P, Greenwood J, Strosberg AD, Cazaubon S, Couraud PO. ICAM-1 signaling pathways associated with Rho activation in microvascular brain endothelial cells. J Immunol 1998;161:5755-5761.
53. Fawcett D. Ultrastructure and function of the Sertoli cell. In: Hamilton D, Greep R (eds). Handbook of Physiology. Washington, DC: American Physiological Society, 1975, 21-25.
54. Fawcett DW. Intercellular bridges. Exp Cell Res 1961;8:174-187.
55. Fawcett DW, Leak LV, Heidger PM. Electron microscopic observations on the structural components of the blood-testis barrier. J Reprod Fertil 1970;(Suppl. 10):105-122.
56. Federici C, Camoin L, Hattab M, Strosberg AD, Couraud PO. Association of the cytoplasmic domain of intercellular-adhesion molecule-1 with glyceraldehyde-3-phosphate dehydrogenase and beta-tubulin. Eur J Biochem 1996;238:173-180.
57. Fernandez-Borja M, van Buul JD, Hordijk PL. The regulation of leucocyte transendothelial migration by endothelial signalling events. Cardiovasc Res 2010; 86:202-210.
58. Fiore E, Fusco C, Romero P, Stamenkovic I. Matrix metalloproteinase 9 (MMP-9/ gelatinase B) proteolytically cleaves ICAM-1 and participates in tumor cell resistance to natural killer cell-mediated cytotoxicity. Oncogene 2002; 21:5213-5223.
59. Franca LR, Auharek SA, Hess RA, Dufour JM, Hinton BT. Blood-tissue barriers: morphofunctional and immunological aspects of the blood-testis and blood- epididymal barriers. Adv Exp Med Biol 2012;763:237-259.
60. Fujita E, Kouroku Y, Ozeki S, Tanabe Y, Toyama Y, Maekawa M, Kojima N, Senoo H, Toshimori K, Momoi T. Oligo-astheno-teratozoospermia in mice lacking RA175/TSLC1/SynCAM/IGSF4A, a cell adhesion molecule in the immunoglobulin superfamily. Mol Cell Biol 2006;26:718-726.
61. Fujita E, Tanabe Y, Hirose T, Aurrand-Lions M, Kasahara T, Imhof BA, Ohno S, Momoi T. Loss of partitioning-defective-3/isotype-specific interacting protein (par-3/ASIP) in the elongating spermatid of RA175 (IGSF4A/SynCAM)- deficient mice. Am J Pathol 2007;171:1800-1810.
62. Furutani Y, Matsuno H, Kawasaki M, Sasaki T, Mori K, Yoshihara Y. Interaction between telencephalin and ERM family proteins mediates dendritic filopodia formation. J Neurosci 2007;27:8866-8876.
63. Gahmberg CG, Tian L, Ning L, Nyman-Huttunen H. ICAM-5-a novel two-facetted adhesion molecule in the mammalian brain. Immunol Lett 2008;117:131-135.
64. Gardel ML, Schneider IC, Aratyn-Schaus Y, Waterman CM. Mechanical integration of actin and adhesion dynamics in cell migration. Annu Rev Cell Dev Biol 2010; 26:315-333.
65. Geijtenbeek TB, Krooshoop DJ, Bleijs DA, van Vliet SJ, van Duijnhoven GC, Grabovsky V, Alon R, Figdor CG, van Kooyk Y. DC-SIGN-ICAM-2 interaction mediates dendritic cell trafficking. Nat Immunol 2000a;1:353-357.
66. Geijtenbeek TB, Torensma R, van Vliet SJ, van Duijnhoven GC, Adema GJ, van Kooyk Y, Figdor CG. Identification of DC-SIGN, a novel dendritic cell-specific ICAM-3 receptor that supports primary immune responses. Cell 2000b;100:575-585.
67. Gerwin N, Gonzalo JA, Lloyd C, Coyle AJ, Reiss Y, Banu N, Wang B, Xu H, Avraham H, Engelhardt B et al. Prolonged eosinophil accumulation in allergic lung interstitium of ICAM-2 deficient mice results in extended hyperresponsiveness. Immunity 1999;10:9-19.
68. Gibson NJ. Cell adhesion molecules in context: CAM function depends on the neighborhood. Cell Adh Migr 2011;5:48-51.
69. Gliki G, Ebnet K, Aurrand-Lions M, Imhof BA, Adams RH. Spermatid differentiation requires the assembly of a cell polarity complex downstream of junctional adhesion molecule-C. Nature 2004;431:320-324.
70. Greenwood J, Amos CL, Walters CE, Couraud PO, Lyck R, Engelhardt B, Adamson P. Intracellular domain of brain endothelial intercellular adhesion molecule-1 is essential for T lymphocyte-mediated signaling and migration. J Immunol 2003;171:2099-2108.
71. Griswold MD. Interactions between germ cells and Sertoli cells in the testis. Biol Reprod 1995;52:211-216.
72. Gurtner GC, Davis V, Li H, McCoy MJ, Sharpe A, Cybulsky MI. Targeted disruption of the murine VCAM1 gene: essential role of VCAM-1 in chorioallantoic fusion and placentation. Genes Dev 1995;9:1-14.
73. Hadad N, Tuval L, Elgazar-Carmom V, Levy R. Endothelial ICAM-1 protein induction is regulated by cytosolic phospholipase A2alpha via both NF-kappaB and CREB transcription factors. J Immunol 2011;186:1816-1827.
74. Harris ES, McIntyre TM, Prescott SM, Zimmerman GA. The leukocyte integrins. J Biol Chem 2000;275:23409-23412.
75. Hayes MJ, Moss SE. Annexin 2 has a dual role as regulator and effector of v-Src in cell transformation. J Biol Chem 2009;284:10202-10210.
76. Hayes MJ, Shao D, Bailly M, Moss SE. Regulation of actin dynamics by annexin 2. EMBO J 2006;25:1816-1826.
77. Hayflick JS, Kilgannon P, Gallatin WM. The intercellular adhesion molecule (ICAM) family of proteins. New members and novel functions. Immunol Res 1998; 17:313-327.
78. Hermand P, Gane P, Huet M, Jallu V, Kaplan C, Sonneborn HH, Cartron JP, Bailly P. Red cell ICAM-4 is a novel ligand for platelet-activated alpha IIbbeta 3 integrin. J Biol Chem 2003;278;4892-4898.
79. Hermo L, Pelletier RM, Cyr DG, Smith CE. Surfing the wave, cycle, life history, and genes/proteins expressed by testicular germ cells. Part 1: background to spermatogenesis, spermatogonia, and spermatocytes. Microsc Res Tech 2010a; 73:241-278.
80. Hermo L, Pelletier RM, Cyr DG, Smith CE. Surfing the wave, cycle, life history, and genes/proteins expressed by testicular germ cells. Part 5: intercellular junctions and contacts between germ cells and Sertoli cells and their regulatory interactions, testicular cholesterol, and genes/proteins associated with more than one germ cell generation. Microsc Res Tech 2010b;73:409-494.
81. Hess RA, de Franca LR. Spermatogenesis and cycle of the seminiferous epithelium. Adv Exp Med Biol 2008;636:1-15.
82. Huang MT, Mason JC, Birdsey GM, Amsellem V, Gerwin N, Haskard DO, Ridley AJ, Randi AM. Endothelial intercellular adhesion molecule (ICAM)-2 regulates angiogenesis. Blood 2005;106:1636-1643.
83. Huang MT, Larbi KY, Scheiermann C, Woodfin A, Gerwin N, Haskard DO, Nourshargh S. ICAM-2 mediates neutrophil transmigration in vivo: evidence for stimulus specificity and a role in PECAM-1-independent transmigration. Blood 2006;107:4721-4727.
84. Hubbard AK, Rothlein R. Intercellular adhesion molecule-1 (ICAM-1) expression and cell signaling cascades. Free Radic Biol Med 2000;28:1379-1386.
85. Igakura T, Kadomatsu K, Kaname T, Muramatsu H, Fan QW, Miyauchi T, Toyama Y, Kuno N, Yuasa S, Takahashi M et al. A null mutation in basigin, an immunoglobulin superfamily member, indicates its important roles in peri-implantation development and spermatogenesis. Dev Biol 1998;194:152-165.
86. Ihanus E, Uotila LM, Toivanen A, Varis M, Gahmberg CG. Red-cell ICAM-4 is a ligand for the monocyte/macrophage integrin CD11c/CD18: characterization of the binding sites on ICAM-4. Blood 2007;109:802-810.
87. Ikeda K, Quertermous T. Molecular isolation and characterization of a soluble isoform of activated leukocyte cell adhesion molecule that modulates endothelial cell function. J Biol Chem 2004;279:55315-55323.
88. Inagaki M, Irie K, Ishizaki H, Tanaka-Okamoto M, Miyoshi J, Takai Y. Role of cell adhesion molecule nectin-3 in spermatid development. Genes Cells 2006; 11:1125-1132.
89. Ivanov AI. Structure and regulation of intestinal epithelial tight junctions. Adv Exp Med Biol 2011;763:132-148.
90. Jean-Mairet RM, Lopez-Menendez C, Sanchez-Ruiloba L, Sacristan S, Rodriguez-Martinez M, Riol-Blanco L, Sanchez-Mateos P, Sanchez-Madrid F, Rodriguez-Fernandez JL, Campanero MR et al. The neuronal protein Kidins220/ARMS associates with ICAM-3 and other uropod components and regulates T-cell motility. Eur J Immunol 2011;41:1035-1046.
91. Juan M, Vinas O, Pino-Otin MR, Places L, Martinez-Caceres E, Barcelo JJ, Miralles A, Vilella R, de la Fuente MA, Vives J et al. CD50 (intercellular adhesion molecule 3) stimulation induces calcium mobilization and tyrosine phosphorylation through p59fyn and p56lck in Jurkat T cell line. J Exp Med 1994;179:1747-1756.
92. Jun CD, Carman CV, Redick SD, Shimaoka M, Erickson HP, Springer TA. Ultrastructure and function of dimeric, soluble intercellular adhesion molecule-1 (ICAM-1). J Biol Chem 2001a;276:29019-29027.
93. Jun CD, Shimaoka M, Carman CV, Takagi J, Springer TA. Dimerization and the effectiveness of ICAM-1 in mediating LFA-1-dependent adhesion. Proc Natl Acad Sci USA 2001b;98:6830-6835.
94. Kammerer S, Roth RB, Reneland R, Marnellos G, Hoyal CR, Markward NJ, Ebner F, Kiechle M, Schwarz-Boeger U, Griffiths LR et al. Large-scale association study identifies ICAM gene region as breast and prostate cancer susceptibility locus. Cancer Res 2004;64:8906-8910.
95. Kang DE, Soriano S, Xia X, Eberhart CG, De Strooper B, Zheng H, Koo EH. Presenilin couples the paired phosphorylation of beta-catenin independent of axin: implications for beta-catenin activation in tumorigenesis. Cell 2002; 110:751-762.
96. Kanters E, van Rijssel J, Hensbergen PJ, Hondius D, Mul FP, Deelder AM, Sonnenberg A, van Buul JD, Hordijk PL. Filamin B mediates ICAM-1-driven leukocyte transendothelial migration. J Biol Chem 2008;283:31830-31839.
97. Kasprzak A, Surdacka A, Tomczak M, Konkol M. Role of high endothelial postcapillary venules and selected adhesion molecules in periodontal diseases: a review. J Periodontal Res 2012 (in press; oi:101111/j1600-0765201201492x).
98. Kevil CG, Orr AW, Langston W, Mickett K, Murphy-Ullrich J, Patel RP, Kucik DF, Bullard DC. Intercellular adhesion molecule-1 (ICAM-1) regulates endothelial cell motility through a nitric oxide-dependent pathway. J Biol Chem 2004; 279:19230-19238.
99. Kim E, Lee Y, Kim JS, Song BS, Kim SU, Huh JW, Lee SR, Kim SH, Hong Y, Chang KT. Extracellular domain of V-set and immunoglobulin domain containing 1 (VSIG1) interacts with sertoli cell membrane protein, while its PDZ-binding motif forms a complex with ZO-1. Mol Cells 2010;30:443-448.
100. Kim K, Brown EE, Choi CB, Alarcon-Riquelme ME, Kelly JA, Glenn SB, Ojwang JO, Adler A, Lee HS, Boackle SA et al. Variation in the ICAM1-ICAM4-ICAM5 locus is associated with systemic lupus erythematosus susceptibility in multiple ancestries. Ann Rheum Dis 2012.
101. Komarova Y, Malik AB. Regulation of endothelial permeability via paracellular and transcellular transport pathways. Annu Rev Physiol 2010;72:463-493.
102. Kuespert K, Pils S, Hauck CR. CEACAMs: their role in physiology and pathophysiology. Curr Opin Cell Biol 2006;18:565-571.
103. Kurio H, Murayama E, Kaneko T, Shibata Y, Inai T, Iida H. Intron retention generates a novel isoform of CEACAM6 that may act as an adhesion molecule in the ectoplasmic specialization structures between spermatids and sertoli cells in rat testis. Biol Reprod 2008;79:1062-1073.
104. Kurio H, Hatsuda H, Murayama E, Kaneko T, Iida H. Identification of CEACAM6 as an intermediate filament-associated protein expressed in Sertoli cells of rat testis. Biol Reprod 2011;85:924-933.
105. Laslett AL, Li LH, Jester WF Jr, Orth JM. Thyroid hormone down-regulates neural cell adhesion molecule expression and affects attachment of gonocytes in Sertoli cell-gonocyte cocultures. Endocrinology 2000;141:1633-1641.
106. Lauke H, Kilic N, Bozorgzad R, Fernando M, Neshat-Vahid S, Pottek T, Ergun S. Expression of carcinoembryonic antigen-related cell adhesion molecule-1 (CEACAM1) in normal human Sertoli cells and its up-regulation in impaired spermatogenesis. Mol Hum Reprod 2004;10:247-252.
107. Lawson C, Ainsworth M, Yacoub M, Rose M. Ligation of ICAM-1 on endothelial cells leads to expression of VCAM-1 via a nuclear factor-kappaB-independent mechanism. J Immunol 1999;162:2990-2996.
108. Leblond C, Clermont Y. Definition of the stages of the cycle of the seminiferous epithelium in the rat. Ann NY Acad Sci 1952a;55:548-573.
109. Leblond CP, Clermont Y. Spermiogenesis of rat, mouse, hamster, and guinea pig as revelaed by the periodic acid-fuchin sulfurous acid technique. Am J Anat 1952b; 90:167-210.
110. Lee NPY, Cheng CY. Ectoplasmic specialization, a testis-specific cell-cell actin-based adherens junction type: is this a potential target for male contraceptive development. Hum Reprod Update 2004;10:349-369.
111. Lee G, Spring FA, Parsons SF, Mankelow TJ, Peters LL, Koury MJ, Mohandas N, Anstee DJ, Chasis JA. Novel secreted isoform of adhesion molecule ICAM-4: potential regulator of membrane-associated ICAM-4 interactions. Blood 2003; 101:1790-1797.
112. Lewis JE, Wahl JK III, Sass KM, Jensen PJ, Johnson KR, Wheelock MJ. Cross-talk between adherens junctions and desmosomes depends on plakoglobin. J Cell Biol 1997;136:919-934.
113. Lie PP, Cheng CY, Mruk DD. The biology of the desmosome-like junction a versatile anchoring junction and signal transducer in the seminiferous epithelium. Int Rev Cell Mol Biol 2011;286:223-269.
114. Lie PP, Cheng CY, Mruk DD. The biology of interleukin-1: emerging concepts in the regulation of the actin cytoskeleton and cell junction dynamics. Cell Mol Life Sci 2012;69:487-500.
115. Lie PP, Xia W, Wang CQ, Mruk DD, Yan HH, Wong CH, Lee WM, Cheng CY. Dynamin II interacts with the cadherin- and occludin-based protein complexes at the blood-testis barrier in adult rat testes. J Endocr 2006;191:571-586.
116. Long EO. ICAM-1: getting a grip on leukocyte adhesion. J Immunol 2011; 186:5021-5023.
117. Lopez-Lerma I, Estrach MT. A distinct profile of serum levels of soluble intercellular adhesion molecule-1 and intercellular adhesion molecule-3 in mycosis fungoides and Sezary syndrome. J Am Acad Dermatol 2009;61:263-270.
118. Luo BH, Carman CV, Springer TA. Structural basis of integrin regulation and signaling. Annu Rev Immunol 2007;25:619-647.
119. Lyck R, Reiss Y, Gerwin N, Greenwood J, Adamson P, Engelhardt B. T-cell interaction with ICAM-1/ICAM-2 double-deficient brain endothelium in vitro: the cytoplasmic tail of endothelial ICAM-1 is necessary for transendothelial migration of T cells. Blood 2003;102:3675-3683.
120. Maekawa M, Ito C, Toyama Y, Suzuki-Toyota F, Fujita E, Momoi T, Toshimori K. Localisation of RA175 (Cadm1), a cell adhesion molecule of the immunoglobulin superfamily, in the mouse testis, and analysis of male infertility in the RA175-deficient mouse. Andrologia 2011;43:180-188.
121. Maness PF, Schachner M. Neural recognition molecules of the immunoglobulin superfamily: signaling transducers of axon guidance and neuronal migration. Nat Neurosci 2007;10:19-26.
122. Mannowetz N, Wandernoth P, Wennemuth G. Basigin interacts with both MCT1 and MCT2 in murine spermatozoa. J Cell Physiol 2012;227:2154-2162.
123. Marambaud P, Shioi J, Serban G, Georgakopoulos A, Sarner S, Nagy V, Baki L, Wen P, Efthimiopoulos S, Shao Z et al. A presenilin-1/gamma-secretase cleavage releases the E-cadherin intracellular domain and regulates disassembly of adherens junctions. EMBO J 2002;21:1948-1956.
124. Martinelli R, Gegg M, Longbottom R, Adamson P, Turowski P, Greenwood J. ICAM-1-mediated endothelial nitric oxide synthase activation via calcium and AMP-activated protein kinase is required for transendothelial lymphocyte migration. Mol Biol Cell 2009;20:995-1005.
125. McCabe SM, Riddle L, Nakamura GR, Prashad H, Mehta A, Berman PW, Jardieu P. sICAM-1 enhances cytokine production stimulated by alloantigen. Cell Immunol 1993;150:364-375.
126. McKinnon PJ, McLaughlin SK, Kapsetaki M, Margolskee RF. Extracellular matrix-associated protein Sc1 is not essential for mouse development. Mol Cell Biol 2000;20:656-660.
127. Mendez MP, Morris SB, Wilcoxen S, Du M, Monroy YK, Remmer H, Murphy H, Christensen PJ, Paine R III. Disparate mechanisms of sICAM-1 production in the peripheral lung: contrast between alveolar epithelial cells and pulmonary microvascular endothelial cells. Am J Physiol Lung Cell Mol Physiol 2008; 294:L807-L814.
128. Millan J, Hewlett L, Glyn M, Toomre D, Clark P, Ridley AJ. Lymphocyte transcellular migration occurs through recruitment of endothelial ICAM-1 to caveola- and F-actin-rich domains. Nat Cell Biol 2006;8:113-123.
129. Miller J, Knorr R, Ferrone M, Houdei R, Carron CP, Dustin ML. Intercellular adhesion molecule-1 dimerization and its consequences for adhesion mediated by lymphocyte function associated-1. J Exp Med 1995;182:1231-1241.
130. Miravet S, Piedra J, Castano J, Raurell I, Franci C, Dunach M, Garcia de Herreros A. Tyrosine phosphorylation of plakoglobin causes contrary effects on its association with desmosomes and adherens junction components and modulates beta-catenin-mediated transcription. Mol Cell Biol 2003; 23:7391-7402.
131. Mirza M, Hreinsson J, Strand ML, Hovatta O, Soder O, Philipson L, Pettersson RF, Sollerbrant K. Coxsackievirus and adenovirus receptor (CAR) is expressed in male germ cells and forms a complex with the differentiation factor JAM-C in mouse testis. Exp Cell Res 2006;312:817-830.
132. Mirza M, Petersen C, Nordqvist K, Sollerbrant K. Coxsackievirus and adenovirus receptor is up-regulated in migratory germ cells during passage of the blood-testis barrier. Endocr 2007;148:5459-5469.
133. Mital P, Hinton BT, Dufour JM. The blood-testis and blood-epididymis barriers are more than just their tight junctions. Biol Reprod 2011;84:851-858.
134. Morrow CMK, Mruk DD, Cheng CY, Hess RA. Claudin and occludin expression and function in the seminiferous epithelium. Philos Trans R Soc Lond B Biol Sci 2010; 365:1679-1696.
135. Mruk DD, Cheng CY. Cell-cell interactions at the ectoplasmic specialization in the testis. Trends Endocrinol Metab 2004a;15:439-447.
136. Mruk DD, Cheng CY. Sertoli-Sertoli and Sertoli-germ cell interactions and their significance in germ cell movement in the seminiferous epithelium during spermatogenesis. Endocr Rev 2004b;25:747-806.
137. Mruk DD, Cheng CY. Desmosomes in the testis: moving into an unchartered territory. Spermatogenesis 2011;1:47-51.
138. Mruk DD, Cheng CY. In search of suitable in vitro models to study germ cell movement across the blood-testis barrier. Spermatogenesis 2012;2:6-10.
139. Mruk DD, Silvestrini B, Cheng CY. Anchoring junctions as drug targets: role in contraceptive development. Pharmacol Rev 2008;60:146-180.
140. Muller WA. Mechanisms of leukocyte transendothelial migration. Annu Rev Pathol 2011;6:323-344.
141. Muro S, Wiewrodt R, Thomas A, Koniaris L, Albelda SM, Muzykantov VR, Koval M. A novel endocytic pathway induced by clustering endothelial ICAM-1 or PECAM-1. J Cell Sci 2003;116:1599-1609.
142. Mustjoki S, Alitalo R, Elonen E, Carpen O, Gahmberg CG, Vaheri A. Intercellular adhesion molecule-1 in extravasation of normal mononuclear and leukaemia cells. Br J Haematol 2001;113:989-1000.
143. Nagamatsu G, Ohmura M, Mizukami T, Hamaguchi I, Hirabayashi S, Yoshida S, Hata Y, Suda T, Ohbo K. A CTX family cell adhesion molecule, JAM4, is expressed in stem cell and progenitor cell populations of both male germ cell and hematopoietic cell lineages. Mol Cell Biol 2006;26:8498-8506.
144. Nalam RL, Lin YN, Matzuk MM. Testicular cell adhesion molecule 1 (TCAM1) is not essential for fertility. Mol Cell Endocr 2010;315:246-253.
145. Nejmeddine M, Negi VS, Mukherjee S, Tanaka Y, Orth K, Taylor GP, Bangham CR. HTLV-1-Tax and ICAM-1 act on T-cell signal pathways to polarize the microtubule-organizing center at the virological synapse. Blood 2009; 114:1016-1025.
146. Nieminen M, Henttinen T, Merinen M, Marttila-Ichihara F, Eriksson JE, Jalkanen S. Vimentin function in lymphocyte adhesion and transcellular migration. Nat Cell Biol 2006;8:156-162.
147. Nottebaum AF, Cagna G, Winderlich M, Gamp AC, Linnepe R, Polaschegg C, Filippova K, Lyck R, Engelhardt B, Kamenyeva O et al. VE-PTP maintains the endothelial barrier via plakoglobin and becomes dissociated from VE-cadherin by leukocytes and by VEGF. J Exp Med 2008;205:2929-2945.
148. Nourshargh S, Hordijk PL, Sixt M. Breaching multiple barriers: leukocyte motility through venular walls and the interstitium. Nat Rev Mol Cell Biol 2010; 11:366-378.
149. Nyman-Huttunen H, Tian L, Ning L, Gahmberg CG. alpha-Actinin-dependent cytoskeletal anchorage is important for ICAM-5-mediated neuritic outgrowth. J Cell Sci 2006;119:3057-3066.
150. O'Donnell L, Nicholls PK, O'Bryan MK, McLachlan RI, Stanton PG. Spermiation: the process of sperm release. Spermatogenesis 2011;1:14-35.
151. Oh HM, Kwon MS, Kim HJ, Jeon BH, Kim HR, Choi HO, Na BR, Eom SH, Song NW, Jun CD. Intermediate monomer-dimer equilibrium structure of native ICAM-1: implication for enhanced cell adhesion. Exp Cell Res 2011; 317:163-172.
152. Ohbo K, Yoshida S, Ohmura M, Ohneda O, Ogawa T, Tsuchiya H, Kuwana T, Kehler J, Abe K, Scholer HR et al. Identification and characterization of stem cells in prepubertal spermatogenesis in mice small star, filled. Dev Biol 2003; 258:209-225.
153. Orth JM, Jester WF, Li LH, Laslett AL. Gonocyte-Sertoli cell interactions during development of the neonatal rodent testis. Curr Top Dev Biol 2000;50:103-124.
154. Otto VI, Heinzel-Pleines UE, Gloor SM, Trentz O, Kossmann T, Morganti-Kossmann MC. sICAM-1 and TNF-alpha induce MIP-2 with distinct kinetics in astrocytes and brain microvascular endothelial cells. J Neurosci Res 2000;60:733-742.
155. Ozaki-Kuroda K, Nakanishi H, Ohta H, Tanaka H, Kurihara H, Mueller S, Irie K, Ikeda W, Sakai T, Wimmer E et al. Nectin couples cell-cell adhesion and the actin scaffold at heterotypic testicular junctions. Curr Biol 2002;12:1145-1150.
156. Park JK, Park SH, So K, Bae IH, Yoo YD, Um HD. ICAM-3 enhances the migratory and invasive potential of human non-small cell lung cancer cells by inducing MMP-2 and MMP-9 via Akt and CREB. Int J Oncol 2010;36:181-192.
157. Parsons JT, Horwitz AR, Schwartz MA. Cell adhesion: integrating cytoskeletal dynamics and cellular tension. Nat Rev Mol Cell Biol 2010;11:633-643.
158. Parvinen M. Regulation of the seminiferous epithelium. Endocr Rev 1982;3:404-417.
159. Pelletier R. The tight junctions in the testis, epididymis, and vas deferens. In: Cereijido M, Anderson J (eds). Tight Junctions. New York: CRC Press, 2001, 599-628.
160. Pelletier RM. The blood-testis barrier: the junctional permeability, the proteins and the lipids. Prog Histochem Cytochem 2011;46:49-127.
161. Pelletier R, Byers S. The blood-testis barrier and Sertoli cell junctions: structural considerations. Microsc Res Tech 1992;20:3-33.
162. Perez OD, Kinoshita S, Hitoshi Y, Payan DG, Kitamura T, Nolan GP, Lorens JB. Activation of the PKB/AKT pathway by ICAM-2. Immunity 2002;16:51-65.
163. Pluskota E, Chen Y, D'Souza SE. Src homology domain 2-containing tyrosine phosphatase 2 associates with intercellular adhesion molecule 1 to regulate cell survival. J Biol Chem 2000;275:30029-30036.
164. Porter JC, Hall A. Epithelial ICAM-1 and ICAM-2 regulate the egression of human T cells across the bronchial epithelium. FASEB J 2009;23:492-502.
165. Rahman A, Fazal F. Hug tightly and say goodbye: role of endothelial ICAM-1 in leukocyte transmigration. Antioxid Redox Signal 2009;11:823-839.
166. Reilly PL, Woska JR Jr, Jeanfavre DD, McNally E, Rothlein R, Bormann BJ. The native structure of intercellular adhesion molecule-1 (ICAM-1) is a dimer. Correlation with binding to LFA-1. J Immunol 1995;155:529-532.
167. Riccioli A, Filippini A, De Cesaris P, Barbacci E, Stefanini M, Starace G, Ziparo E. Inflammatory mediators increase surface expression of integrin ligands, adhesion to lymphocytes, and secretion of interleukin 6 in mouse Sertoli cells. Proc Natl Acad Sci USA 1995;92:5808-5812.
168. Robledo O, Papaioannou A, Ochietti B, Beauchemin C, Legault D, Cantin A, King PD, Daniel C, Alakhov VY, Potworowski EF et al. ICAM-1 isoforms: specific activity and sensitivity to cleavage by leukocyte elastase and cathepsin G. Eur J Immunol 2003;33:1351-1360.
169. Rodriguez-Fernandez JL, Gomez M, Luque A, Hogg N, Sanchez-Madrid F, Cabanas C. The interaction of activated integrin lymphocyte function-associated antigen 1 with ligand intercellular adhesion molecule 1 induces activation and redistribution of focal adhesion kinase and proline-rich tyrosine kinase 2 in T lymphocytes. Mol Biol Cell 1999;10:1891-1907.
170. Russell L. Movement of spermatocytes from the basal to the adluminal compartment of the rat testis. Am J Anat 1977;148:313-328.
171. Russell L, Clermont Y. Anchoring device between Sertoli cells and late spermatids in rat seminiferous tubules. Anat Rec 1976;185:259-278.
172. Russell LD. The blood-testis barrier and its formation relative to spermatocyte maturation in the adult rat: a lanthanum tracer study. Anat Rec 1978;190:99-111.
173. Russell LD, Peterson RN. Sertoli cell junctions: morphological and functional correlates. Int Rev Cytol 1985;94:177-211.
174. Russell LD, Saxena NK, Turner TT. Cytoskeletal involvement in spermiation and sperm transport. Tissue Cell 1989;21:361-379.
175. Sakaguchi T, Nishimoto M, Miyagi S, Iwama A, Morita Y, Iwamori N, Nakauchi H, Kiyonari H, Muramatsu M, Okuda A. Putative "stemness" gene jam-B is not required for maintenance of stem cell state in embryonic, neural, or hematopoietic stem cells. Mol Cell Biol 2006; 26:6557-6570.
176. Sakatani S, Takahashi R, Okuda Y, Aizawa A, Otsuka A, Komatsu A, Ono M. Structure, expression, and conserved physical linkage of mouse testicular cell adhesion molecule-1 (TCAM-1) gene. Genome 2000;43:957-962.
177. Sarkar O, Xia W, Mruk DD. Adjudin-mediated junction restructuring in the seminiferous epithelium leads to displacement of soluble guanylate cyclase from adherens junctions. J Cell Physiol 2006;208:175-187.
178. Sato H, Azuma Y, Higai K, Matsumoto K. Altered expression of glycoproteins on the cell surface of Jurkat cells during etoposide-induced apoptosis: shedding and intracellular translocation of glycoproteins. Biochim Biophys Acta 2009; 1790:1198-1205.
179. Schenkel AR, Mamdouh Z, Muller WA. Locomotion of monocytes on endothelium is a critical step during extravasation. Nat Immunol 2004;5:393-400.
180. Schnoor M, Lai FP, Zarbock A, Klaver R, Polaschegg C, Schulte D, Weich HA, Oelkers JM, Rottner K, Vestweber D. Cortactin deficiency is associated with reduced neutrophil recruitment but increased vascular permeability in vivo. J Exp Med 2011;208:1721-1735.
181. Serrador JM, Vicente-Manzanares M, Calvo J, Barreiro O, Montoya MC, Schwartz-Albiez R, Furthmayr H, Lozano F, Sanchez-Madrid F. A novel serine-rich motif in the intercellular adhesion molecule 3 is critical for its ezrin/ radixin/moesin-directed subcellular targeting. J Biol Chem 2002; 277:10400-10409.
182. Serrano D, Bhowmick T, Chadha R, Garnacho C, Muro S. Intercellular adhesion molecule 1 engagement modulates sphingomyelinase and ceramide, supporting uptake of drug carriers by the vascular endothelium. Arterioscler Thromb Vasc Biol 2012;32:1178-1185.
183. Setchell B. Sermatogenesis. In: Finn C (ed.). The Mammalian Testis. New York: Cornell University Press, 1978, 181-232.
184. Setchell BP. The Functional Significance of the Blood-testis Barrier. Journal of Andrology 1980;1:3-10.
185. Setchell BP. Blood-testis barrier, functional and transport proteins and spermatogenesis. Adv Exp Med Biol 2008;636:212-233.
186. Setchell BP, Waites GMH. Changes in the permeability of the testicular capillaries and of the 'blood-testis barrier' after injection of cadmium chloride in the rat. J Endocrinol 1970;47:81-86.
187. Setchell BP, Waites GMB. The blood-testis barrier. In: Hamilton DW, Greep RO (eds). The Handbook of Physiology Section 7, Vol. V Male Reproductive System. Washington, D.C: American Physiological Society, 1975, 143-172.
188. Shaha C, Tripathi R, Mishra DP. Male germ cell apoptosis: regulation and biology. Philos Trans R Soc Lond B Biol Sci 2010;365:1501-1515.
189. Shao M, Ghosh A, Cooke VG, Naik UP, Martin-DeLeon PA. JAM-A is present in mammalian spermatozoa where it is essential for normal motility. Dev Biol 2008;313:246-255.
190. Shaw SK, Bamba PS, Perkins BN, Luscinskas FW. Real-time imaging of vascular endothelial-cadherin during leukocyte transmigration across endothelium. J Immunol 2001;167:2323-2330.
191. Shaw SK, Ma S, Kim MB, Rao RM, Hartman CU, Froio RM, Yang L, Jones T, Liu Y, Nusrat A et al. Coordinated redistribution of leukocyte LFA-1 and endothelial cell ICAM-1 accompany neutrophil transmigration. J Exp Med 2004;200:1571-1580.
192. Shen L, Weber CR, Raleigh DR, Yu D, Turner JR. Tight junction pore and leak pathways: a dynamic duo. Annu Rev Physiol 2011;73:283-309.
193. Sithu SD, English WR, Olson P, Krubasik D, Baker AH, Murphy G, D'Souza SE. Membrane-type 1-matrix metalloproteinase regulates intracellular adhesion molecule-1 (ICAM-1)-mediated monocyte transmigration. J Biol Chem 2007; 282:25010-25019.
194. Siu E, Wong E, Mruk D, Porto C, Cheng C. Focal adhesion kinase is a blood-testis barrier regulator. Proc Natl Acad Sci USA 2009;106:9298-9303.
195. Sligh JE Jr, Ballantyne CM, Rich SS, Hawkins HK, Smith CW, Bradley A, Beaudet AL. Inflammatory and immune responses are impaired in mice deficient in intercellular adhesion molecule 1. Proc Natl Acad Sci USA 1993;90:8529-8533.
196. Smith A, Bracke M, Leitinger B, Porter JC, Hogg N. LFA-1-induced T cell migration on ICAM-1 involves regulation of MLCK-mediated attachment and ROCK-dependent detachment. J Cell Sci 2003;116:3123-3133.
197. Spring FA, Parsons SF, Ortlepp S, Olsson ML, Sessions R, Brady RL, Anstee DJ. Intercellular adhesion molecule-4 binds alpha(4)beta(1) and alpha(V)-family integrins through novel integrin-binding mechanisms. Blood 2001;98:458-466.
198. Steiner O, Coisne C, Cecchelli R, Boscacci R, Deutsch U, Engelhardt B, Lyck R. Differential roles for endothelial ICAM-1, ICAM-2, and VCAM-1 in shear-resistant T cell arrest, polarization, and directed crawling on blood-brain barrier endothelium. J Immunol 2010;185:4846-4855.
199. Strell C, Lang K, Niggemann B, Zaenker KS, Entschladen F. Neutrophil granulocytes promote the migratory activity of MDA-MB-468 human breast carcinoma cells via ICAM-1. Exp Cell Res 2010;316:138-148.
200. Su L, Cheng CY, Mruk DD. Drug transporter, P-glycoprotein (MDR1), is an integrated component of the mammalian blood-testis barrier. Int J Biochem Cell Biol 2009;41:2578-2587.
201. Su W, Mruk DD, Cheng CY, Filamin A. A regulator of blood-testis barrier assembly during post-natal development. Spermatogenesis 2012;2:73-78.
202. Sumagin R, Sarelius IH. A role for ICAM-1 in maintenance of leukocyte-endothelial cell rolling interactions in inflamed arterioles. Am J Physiol Heart Circ Physiol 2007; 293:H2786-2798.
203. Sumagin R, Sarelius IH. Intercellular adhesion molecule-1 enrichment near tricellular endothelial junctions is preferentially associated with leukocyte transmigration and signals for reorganization of these junctions to accommodate leukocyte passage. J Immunol 2010;184:5242-5252.
204. Sumagin R, Kuebel JM, Sarelius IH. Leukocyte rolling and adhesion both contribute to regulation of microvascular permeability to albumin via ligation of ICAM-1. Am J Physiol Cell Physiol 2011;301:C804-C813.
205. Taddei ML, Giannoni E, Fiaschi T, Chiarugi P. Anoikis: an emerging hallmark in health and diseases. J Pathol 2012;226:380-393.
206. Takai Y, Ikeda W, Ogita H, Rikitake Y. The immunoglobulin-like cell adhesion molecule nectin and its associated protein afadin. Annu Rev Cell Dev Biol 2008; 24:309-342.
207. Tarin C, Gomez M, Calvo E, Lopez JA, Zaragoza C. Endothelial nitric oxide deficiency reduces MMP-13-mediated cleavage of ICAM-1 in vascular endothelium: a role in atherosclerosis. Arterioscler Thromb Vasc Biol 2009; 29:27-32.
208. Tarulli GA, Meachem SJ, Schlatt S, Stanton PG. Regulation of testicular tight junctions by gonadotrophins in the adult Djungarian hamster in vivo. Reprod 2008; 135:867-877.
209. Terada N, Ohno N, Saitoh S, Saitoh Y, Komada M, Kubota H, Ohno S. Involvement of a membrane skeletal protein, 4.1G, for Sertoli/germ cell interaction. Reprod 2010;139:883-892.
210. Thomas S, Baumgart DC. Targeting leukocyte migration and adhesion in Crohn's disease and ulcerative colitis. Inflammopharmacol 2012;20:1-18.
211. Thompson PW, Randi AM, Ridley AJ. Intercellular adhesion molecule (ICAM)-1, but not ICAM-2, activates RhoA and stimulates c-fos and rhoA transcription in endothelial cells. J Immunol 2002;169:1007-1013.
212. Tian L, Stefanidakis M, Ning L, Van Lint P, Nyman-Huttunen H, Libert C, Itohara S, Mishina M, Rauvala H, Gahmberg CG. Activation of NMDA receptors promotes dendritic spine development through MMP-mediated ICAM-5 cleavage. J Cell Biol 2007;178:687-700.
213. Tilghman RW, Hoover RL. The Src-cortactin pathway is required for clustering of E-selectin and ICAM-1 in endothelial cells. FASEB J 2002;16:1257-1259.
214. Topp SA, Upadhya GA, Strasberg SM. Leukocyte adhesion to cold-preserved rat endothelial cells: role of actin disassembly and ICAM-1. Liver Transpl 2003; 9:1286-1294.
215. Toyama Y, Maekawa M, Kadomatsu K, Miyauchi T, Muramatsu T, Yuasa S. Histological characterization of defective spermatogenesis in mice lacking the basigin gene. Anat Histol Embryol 1999;28:205-213.
216. Toyama Y, Maekawa M, Yuasa S. Ectoplasmic specializations in the Sertoli cells: new vistas based on genetic defects and testicular toxicology. Anat Sci Int 2003; 78:1-16.
217. Trinh-Trang-Tan MM, Vilela-Lamego C, Picot J, Wautier MP, Cartron JP. Intercellular adhesion molecule-4 and CD36 are implicated in the abnormal adhesiveness of sickle cell SAD mouse erythrocytes to endothelium. Haematologica 2010; 95:730-737.
218. Tsakadze NL, Sen U, Zhao Z, Sithu SD, English WR, D'Souza SE. Signals mediating cleavage of intercellular adhesion molecule-1. Am J Physiol Cell Physiol 2004; 287:C55-63.
219. Tsakadze NL, Sithu SD, Sen U, English WR, Murphy G, D'Souza SE. Tumor necrosis factor-alpha-converting enzyme (TACE/ADAM-17) mediates the ectodomain cleavage of intercellular adhesion molecule-1 (ICAM-1). J Biol Chem 2006; 281:3157-3164.
220. Tse MC, Lane C, Mott K, Onlamoon N, Hsiao HM, Perng GC. ICAM-5 modulates cytokine/chemokine production in the CNS during the course of herpes simplex virus type 1 infection. J Neuroimmunol 2009;213:12-19.
221. Turowski P, Martinelli R, Crawford R, Wateridge D, Papageorgiou AP, Lampugnani MG, Gamp AC, Vestweber D, Adamson P, Dejana E et al. Phosphorylation of vascular endothelial cadherin controls lymphocyte emigration. J Cell Sci 2008;121:29-37.
222. van Den Engel NK, Heidenthal E, Vinke A, Kolb H, Martin S. Circulating forms of intercellular adhesion molecule (ICAM)-1 in mice lacking membranous ICAM-1. Blood 2000;95:1350-1355.
223. van Buul JD, Voermans C, van den Berg V, Anthony EC, Mul FP, vanWetering S, van der Schoot CE, Hordijk PL. Migration of human hematopoietic progenitor cells across bone marrow endothelium is regulated by vascular endothelial cadherin. J Immunol 2002;168:588-596.
224. van Buul JD, Allingham MJ, Samson T, Meller J, Boulter E, Garcia-Mata R, Burridge K. RhoG regulates endothelial apical cup assembly downstream from ICAM1 engagement and is involved in leukocyte trans-endothelial migration. J Cell Biol 2007;178:1279-1293.
225. van Buul JD, van Rijssel J, van Alphen FP, Hoogenboezem M, Tol S, Hoeben KA, van Marle J, Mul EP, Hordijk PL. Inside-out regulation of ICAM-1 dynamics in TNF-alpha-activated endothelium. PLoS ONE 2010a;5:e11336.
226. van Buul JD, van Rijssel J, van Alphen FP, van Stalborch AM, Mul EP, Hordijk PL. ICAM-1 clustering on endothelial cells recruits VCAM-1. J Biomed Biotechnol 2010b;2010:120328.
227. van Rijssel J, Kroon J, Hoogenboezem M, van Alphen FP, de Jong RJ, Kostadinova E, Geerts D, Hordijk PL, van Buul JD. The Rho-guanine nucleotide exchange factor Trio controls leukocyte transendothelial migration by promoting docking structure formation. Mol Biol Cell 2012;23:2831-2844.
228. Vicente-Manzanares M, Sanchez-Madrid F. Role of the cytoskeleton during leukocyte responses. Nat Rev Immunol 2004;4:110-122.
229. Vogl A, Pfeiffer D, Redenbach D. Ectoplasmic ('junctional') specializations in mammalian Sertoli cells: influence on spermatogenic cells. Ann NY Acad Sci 1991;637:175-202.
230. Vogl A, Pfeiffer D, Redenbach D, Grove B. Sertoli cell cytoskeleton. In: Russell L, Griswold M (eds). The Sertoli Cell. Clearwater: Cache River Press, 1993, 39-86.
231. Vogl A, Pfeiffer D, Mulholland D, Kimel G, Guttman J. Unique and multifunctional adhesion junctions in the testis: ectoplasmic specializations. Arch Histol Cytol 2000;63:1-15.
232. Vogl AW, Vaid KS, Guttman JA. The Sertoli cell cytoskeleton. Adv Exp Med Biol 2008;636:186-211.
233. Wakayama T, Sai Y, Ito A, Kato Y, Kurobo M, Murakami Y, Nakashima E, Tsuji A, Kitamura Y, Iseki S. Heterophilic binding of the adhesion molecules poliovirus receptor and immunoglobulin superfamily 4A in the interaction between mouse spermatogenic and Sertoli cells. Biol Reprod 2007;76:1081-1090.
234. Wang Q, Pfeiffer GR II, Gaarde WA. Activation of SRC tyrosine kinases in response to ICAM-1 ligation in pulmonary microvascular endothelial cells. J Biol Chem 2003; 278:47731-47743.
235. Wang HW, Babic AM, Mitchell HA, Liu K, Wagner DD. Elevated soluble ICAM-1 levels induce immune deficiency and increase adiposity in mice. FASEB J 2005; 19:1018-1020.
236. Wang CQ, Cheng CY. A seamless trespass: germ cell migration across the seminiferous epithelium during spermatogenesis. J Cell Biol 2007;178:549-556.
237. Wang CQ, Mruk DD, Lee WM, Cheng CY. Coxsackie and adenovirus receptor (CAR) is a product of Sertoli and germ cells in rat testes which is localized at the Sertoli-Sertoli and Sertoli-germ cell interface. Exp Cell Res 2007;313: 1373-1392.
238. Wang Y, Lui WY. Opposite effects of interleukin-1a and transforming growth factor-b2 induce stage-specific regulation of junctional adhesion molecule-B gene in Sertoli cells. Endocr 2009;150:2404-2412.
239. Weber JE, Russell LD, Wong V, Peterson RN. Three-dimensional reconstruction of a rat stage V Sertoli cell: II. Morphometry of Sertoli-Sertoli and Sertoli- germ-cell relationships. Am J Anat 1983;167:163-179.
240. Weber GF, Bjerke MA, DeSimone DW. Integrins and cadherins join forces to form adhesive networks. J Cell Sci 2011;124:1183-1193.
241. Welder CA, Lee DH, Takei F. Inhibition of cell adhesion by microspheres coated with recombinant soluble intercellular adhesion molecule-1. J Immunol 1993; 150:2203-2210.
242. Whittard JD, Craig SE, Mould AP, Koch A, Pertz O, Engel J, Humphries MJ. E-cadherin is a ligand for integrin alpha2beta1. Matrix Biol 2002;21:525-532.
243. Witkowska AM, Borawska MH. Soluble intercellular adhesion molecule-1 (sICAM-1): an overview. Eur Cytokine Netw 2004;15:91-98.
244. Wittchen ES. Endothelial signaling in paracellular and transcellular leukocyte transmigration. Front Biosci 2009;14:2522-2545.
245. Wong CH, Mruk DD, Lui WY, Cheng CY. Regulation of blood-testis barrier dynamics: an in vivo study. J Cell Sci 2004;117:783-798.
246. Wong EWP, Mruk DD, Cheng CY. Biology and regulation of ectoplasmic specialization, an atypical adherens junction type, in the testis. Biochem Biophys Acta 2008;1778:692-708.
247. Woodfin A, Voisin MB, Imhof BA, Dejana E, Engelhardt B, Nourshargh S. Endothelial cell activation leads to neutrophil transmigration as supported by the sequential roles of ICAM-2, JAM-A, and PECAM-1. Blood 2009;113:6246-6257.
248. Xia W, Mruk DD, Cheng CY. C-type natriuretic peptide regulates blood-testis barrier dynamics in adult rat testes. Proc Natl Acad Sci USA 2007;104:3841-3846.
249. XiaW, Wong EW, Mruk DD, Cheng CY. TGF-beta3 and TNFalpha perturb blood- testis barrier (BTB) dynamics by accelerating the clathrin-mediated endocytosis of integral membrane proteins: a new concept of BTB regulation during spermatogenesis. Dev Biol 2009;327:48-61.
250. Xiao X, Mruk DD, Lee WM, Cheng CY. c-Yes regulates cell adhesion at the blood- testis barrier and the apical ectoplasmic specialization in the seminiferous epithelium of rat testes. Int J Biochem Cell Biol 2011;43:651-665.
251. Xiao X, Cheng CY, Mruk DD. Intercellular adhesion molecule (ICAM)-1 is a regulator of blood-testis barrier function. J Cell Sci 2012a (in press; doi:10.1242/jcs107987; PMID:22976294).
252. Xiao X, Cheng CY, Mruk DD. Intercellular adhesion molecule (ICAM)-2 is involved in apical ectoplasmic specialization dynamics during spermatogenesis in the rat. J Endocr 2012b (in press; doi:10.1530/JOE-12-0434; PMID:23097088).
253. Yan HHN, Mruk DD, Lee WM, Cheng CY. Ectoplasmic specialization: a friend or a foe of spermatogenesis? BioEssays 2007;29:36-48.
254. Yan HHN, Mruk DD, Cheng CY. Junction restructuring and spermatogenesis: the biology, regulation, and implication in male contraceptive development. Curr Top Dev Biol 2008;80:57-92.
255. Yang Y, Han C. GDNF stimulates the proliferation of cultured mouse immature Sertoli cells via its receptor subunit NCAM and ERK1/2 signaling pathway. BMC Cell Biol 2010;11:78.
256. Yang Y, Jun CD, Liu JH, Zhang R, Joachimiak A, Springer TA, Wang JH. Structural basis for dimerization of ICAM-1 on the cell surface. Mol Cell 2004;14:269-276.
257. Yang L, Froio RM, Sciuto TE, Dvorak AM, Alon R, Luscinskas FW. ICAM-1 regulates neutrophil adhesion and transcellular migration of TNF-alpha-activated vascular endothelium under flow. Blood 2005;106:584-592.
258. Yang L, Kowalski JR, Yacono P, Bajmoczi M, Shaw SK, Froio RM, Golan DE, Thomas SM, Luscinskas FW. Endothelial cell cortactin coordinates intercellular adhesion molecule-1 clustering and actin cytoskeleton remodeling during polymorphonuclear leukocyte adhesion and transmigration. J Immunol 2006; 177:6440-6449.
259. Yang S, Weng H, Chen L, Guo X, Parra M, Conboy J, Debnath G, Lambert AJ, Peters LL, Baines AJ et al. Lack of protein 4.1G causes altered expression and localization of the cell adhesion molecule nectin-like 4 in testis and can cause male infertility. Mol Cell Biol 2011;31:2276-2286.
260. Yazama F. Continual maintenance of the blood-testis barrier during spermatogenesis: the intermediate compartment theory revisited. J Reprod Dev 2008;54:299-305.
261. Yoon KJ, Phelps DA, Bush RA, Remack JS, Billups CA, Khoury JD. ICAM-2 expression mediates a membrane-actin link, confers a nonmetastatic phenotype and reflects favorable tumor stage or histology in neuroblastoma. PLoS One 2008;3:e3629.
262. Young JS, Vogl AW. Focal adhesion proteins zyxin and vinculin are co-distributed at tubulobulbar complexes. Spermatogenesis 2012;2:63-68.
263. Young JS, Guttman JA, Vaid KS, Vogl AW. Cortactin (CTTN), N-WASP (WASL), and clathrin (CLTC) are present at podosome-like tubulobulbar complexes in the rat testis. Biol Reprod 2009a;80:153-161.
264. Young JS, Guttman JA, Vaid KS, Vogl AW. Tubulobulbar complexes are intercellular podosome-like structures that internalize intact intercellular junctions during epithelial remodeling events in the rat testis. Biol Reprod 2009b;80:162-174.
265. Young JS, Takai YK, Kojic KL, Vogl AW. Internalization of adhesion junction proteins and their association with recycling endosome marker proteins in rat seminiferous epithelium. Reproduction 2012;143:347-357.
266. Yuasa J, Toyama Y, Miyauchi T, Maekawa M, Yuasa S, Ito H. Specific localization of the basigin protein in human testes from normal adults, normal juveniles, and patients with azoospermia. Andrologia 2001;33:293-299.
267. Zennadi R, Hines PC, De Castro LM, Cartron JP, Parise LV, Telen MJ. Epinephrine acts through erythroid signaling pathways to activate sickle cell adhesion to endothelium via LW-alphavbeta3 interactions. Blood 2004;104: 3774-3781.