Rat glomerular mesangial cells require laminin-9 to migrate in response to insulin-like growth factor binding protein-5

American Journal of Physiology - Cell Physiology

Volumn 291, Issue 4, 2006, Pages

  Berfield, Anne K ^a   Hansen, Kim M ^a   Abrass, Christine K ^b,c  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b VA PUGET SOUND HEALTH CARE SYSTEM   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Extracellular matrix; Integrins; Migration

Indexed keywords

LAMININ; MESSENGER RNA; OLIGONUCLEOTIDE; PROTEIN LAMA4; PROTEIN LAMB2; PROTEIN LAMC1; PROTEIN LAMININ 9; SOMATOMEDIN BINDING PROTEIN 5; UNCLASSIFIED DRUG; VERY LATE ACTIVATION ANTIGEN 6;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; EXTRACELLULAR MATRIX; MESANGIUM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; RAT;

ANIMALS; CELL MEMBRANE; CELL MOVEMENT; CELLS, CULTURED; INSULIN-LIKE GROWTH FACTOR BINDING PROTEIN 5; INTEGRIN ALPHA6BETA1; LAMININ; MESANGIAL CELLS; OLIGONUCLEOTIDES, ANTISENSE; RATS; RNA, MESSENGER;

EID: 33749327324     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00623.2005     Document Type: Article

References (66)

1. Abrass CK, Berfield AK, and Andress DL. Heparin binding domain of insulin-like growth factor binding protein-5 stimulates mesangial cell migration. Am J Physiol Renal Physiol 273: F899-F906, 1997.
2. Abrass CK, Spicer D, Berfield AK, St. John PL, and Abrahamson DR. Diabetes induces changes in glomerular development and laminin β2 (s-laminin) expression. Am J Pathol 151: 1131-1140, 1997.
3. Abrass CK, Spicer D, and Raugi GJ. Insulin induces a change in extracellular matrix glycoproteins synthesized by rat mesangial cells in culture. Kidney Int 46: 613-620, 1994.
4. Abrass CK, Spicer D, and Raugi GJ. Induction of nodular sclerosis by insulin in rat mesangial cells in vitro: studies of collagen. Kidney Int 47: 25-37, 1995.
5. Arar M, Xu YC, Elshihabi I, Barnes JL, Choudhury GG, and Abboud HE. Platelet-derived growth factor receptor beta regulates migration and synthesis in metanephric mesenchymal cells. J Biol Chem 275: 9527-9533, 2000.
6. Aumailley M, Bruckner-Tuderman L, Carter WG, Deutzmann R, Edgar D, Ekblom P, Engel J, Engvall E, Hohenester E, Jones JCR, Kleinman H, Marinkovich MP, Martin GR, Mayer U, Meneguzzi G, Miner JH, Miyazaki K, Patarroyo M, Paulsson M, Quaranta V, Sanes JR, Sasaki T, Sekiguchi K, Sorokin L, Talts JF, Tryggvason K, Uitto J, Virtanen I, Von der Mark H, Wewer UM, Yamada Y, and Yurchenco P. A simplified laminin nomenclature. Matrix Biol 24: 326-332, 2005.
7. 201-218 stimulates Cdc42 aggregation and filopodia formation in migrating mesangial cells. Kidney Int 57: 1991-2003, 2000.
8. Berfield AK, Andress DL, and Abrass CK. IGF-1-induced lipid accumulation impairs mesangial cell migration and contractile function. Kidney Int 62: 1229-1237, 2002.
9. Berfield AK, Spicer D, and Abrass CK. Insulin-like growth factor I (IGF-I) induces unique effects in the cytoskeleton of cultured rat glomerular mesangial cells. J Histochem Cytochem 45: 583-593, 1997.
10. Bjarnegard M, Enge M, Norlin J, Gustafsdottir S, Fredriksson S, Abramsson A, Takemoto M, Gustafsson E, Fassler R, and Betsholtz C. Endothelium-specific ablation of PDGFB leads to pericyte loss and glomerular, cardiac and placental abnormalities. Development 131: 1847-1857, 2004.
11. Butt AJ, Dickson KA, McDougall F, and Baxter RC. Insulin-like growth factor-binding protein-5 inhibits the growth of human breast cancer cells in vitro and in vivo. J Biol Chem 278: 29676-29685, 2003.
12. Chai Q, Krag S, Miner JH, Nyengaard JR, Chai S, and Wogensen L. TGF-β1 induces aberrant laminin chain and collagen type IV isotype expression in the glomerular basement membrane. Nephron Exper Nephrol 94: E123-E136, 2003.
13. 1 integrin. J Cell Biol 115: 843-850, 1991.
14. Couchman JR and Woods A. Syndecan-4 and integrins: combinatorial signaling in cell adhesion. J Cell Sci 112: 3415-3420, 1999.
15. DeHahn KC, Gonzales M, Gonzalez AM, Hopkinson SB, Chandel NS, Brunelle JK, and Jones JC. The α4 laminin subunit regulates endothelial cell survival. Exp Cell Res 294: 281-289, 2004.
16. Durbeej M, Henry MD, Ferletta M, Campbell KP, and Ekblom P. Distribution of dystroglycan in normal adult mouse tissues. J Histochem Cytochem 46: 449-457, 1998.
17. Ferletta M, Kikkawa Y, Yu H, Talts JF, Durbeej M, Sonnenberg A, Timpl R, Campbell KP, Ekblom P, and Genersch E. Opposing roles of integrin α6Aβ1 and dystroglycan in laminin-mediated extracellular signal-regulated kinase activation. Mol Biol Cell 14: 2088-2103, 2003.
18. French-Constant C and Colognato H. Integrins: versatile integrators of extracellular signals. Trends Cell Biol 14: 678-686, 2004.
19. Fujiwara H, Gu J, and Sekiguchi K. Rac regulates integrin-mediated endothelial cell adhesion and migration on laminin-8. Exp Cell Res 292: 67-77, 2003.
20. Fujiwara H, Kikkawa Y, Sanzen N, and Sekiguchi K. Purification and characterization of human laminin-8. Laminin-8 stimulates cell adhesion and migration through α3β1 and α6β1 integrins. J Biol Chem 276: 17550-17558, 2001.
21. Gebarowska D, Stitt AW, Gardiner TA, Harriott P, Greer B, and Nelson J. Synthetic peptides interacting with the 67-kd laminin receptor can reduce retinal ischemia and inhibit hypoxia-induced retinal neovascularization. Am J Pathol 160: 307-313, 2002.
22. Geberhiwot T, Assefa D, Kortesmaa J, Ingerpuu S, Pedraza C, Wondimu Z, Charo J, Kiessling R, Virtanen I, Tryggvason K, and Patarroyo M. Laminin-8 (α4β1γ1) is synthesized by lymphoid cells, promotes lymphocyte migration and costimulates T cell proliferation. J Cell Sci 114: 423-433, 2001.
23. Gleave M and Jansen B. Clusterin and IGFBPs as antisense targets in prostate cancer. Ann NY Acad Sci 1002: 95-104, 2003.
24. Goel HL, Fornaro M, Moro L, Teider N, Rhim JS, King M, and Languino LR. Selective modulation of type 1 insulin-like growth factor receptor signaling and functions by β1 integrins. J Cell Biol 166: 407-418, 2004.
25. Gonzales M, Weksler B, Tsuruta D, Goldman RD, Yoon KJ, Hopkinson SB, Flitney FW, and Jones JCR. Structure and function of a vimentin-associated matrix adhesion in endothelial cells. Mol Biol Cell 12: 85-100, 2001.
26. Gonzalez AM, Gonzalez M, Herron GS, Nagavarapu U, Hopkinson SB, Tsuruta D, and Jones JCR. Complex interactions between the laminin α4 subunit and integrins regulate endothelial cell behavior in vitro and angiogenesis in vivo. Proc Natl Acad Sci USA 99: 16075-16080, 2002.
27. Hansen K and Abrass CK. Role of laminin isoforms in glomerular structure. Pathobiology 67: 84-91, 1999.
28. Hansen K, Berfield AK, Spicer D, and Abrass CK. Rat mesangial cells express two unique isoforms of laminin which modulate mesangial cell phenotype. Matrix Biol 17: 117-130, 1998.
29. Hansen KM and Abrass CK. Laminin-8/9 is synthesized by rat glomerular mesangial cells and is required for PDGF-induced mesangial cell migration. Kidney Int 64: 110-118, 2003.
30. Henry MD, Satz JS, Brakebusch C, Costell M, Gustafsson E, Fässler R, and Campbell KP. Distinct roles for dystroglycan, β1 integrin and perlecan in cell surface laminin organization. J Cell Sci 114: 1137-1144, 2005.
31. Hsieh T, Gordon RE, Clemmons DR, Busby WH Jr, and Duan C. Regulation of vascular smooth muscle cell responses to insulin-like growth factor (IGF)-I by local IGF-binding proteins. J Biol Chem 278: 42886-42892, 2003.
32. Hugo C, Shankland SJ, Bowen-Pope DF, Couser WG, and Johnson RJ. Extraglomerular origin of the mesangial cell after injury. J Clin Invest 223: 72-82, 1997.
33. Ido H, Harada K, Futaki S, Hayashi Y, Nishiuchi R, Natsuka Y, Li S, Wada Y, Combs AC, Ervasti JM, and Sekiguchi K. Molecular dissection of the α-dystroglycan- and integrin-binding sites within the globular domain of human laminin-10. J Biol Chem 279: 10946-10954, 2004.
34. Jones JI, Prevette T, Gockerman A, and Clemmons DR. Ligand occupancy of the αVβ3 integrin is necessary for smooth muscle cells to migrate in response to insulin-like growth factor I. Proc Natl Acad Sci USA 93: 2482-2487, 1996.
35. Kashtan CE, Kim Y, Lees GE, Thorner PS, Virtanen I, and Miner JH. Abnormal glomerular basement membrane laminins in murine, canine, and human Alport syndrome: Aberrant laminin α2 deposition is species independent. J Am Soc Nephrol 12: 252-260, 2001.
36. Khazenzon NM, Ljubimov AV, Lakhtar AJ, Fujita M, Fujiwara H, Sekiguchi K, Sorokin LM, Petäjäniemi N, Virtanen I, Black KL, and Ljubimova JY. Antisense inhibition of laminin-8 expression reduces invasion of human gliomas in vitro. Mol Cancer Ther 2: 985-994, 2003.
37. Kikkawa Y, Virtanen I, and Miner JH. Mesangial cells organize the glomerular capillaries by adhering to the G domain of laminin α5 in the glomerular basement membrane. J Cell Biol 161: 187-196, 2003.
38. Kortesmaa J, Yurchenco P, and Tryggvason K. Recombinant laminin-8 (α4β1γ1) production, purification, and interactions with integrins. J Biol Chem 275: 14853-14859, 2000.
39. Kreisberg JI and Karnovsky MJ. Glomerular cells in culture. Kidney Int 23: 439-447, 1983.
40. Langhofer M, Hopkinson SB, and Jones JCR. The matrix secreted by 804G cells contains laminin-related components that participate in hemidesmosome assembly in vitro. J Cell Sci 105: 753-764, 1993.
41. Lindblom P, Gerhardt H, Liebner S, Abramsson A, Enge M, Hellstrom M, Backstrom G, Fredriksson S, Landegren U, Nystrom HC, Bergstrom G, Dejana E, Ostman A, Lindahl P, and Betsholtz C. Endothelial PDGF-B retention is required for proper investment of pericytes in the microvessel wall. Genes Dev 17: 1835-1840, 2003.
42. Ljubimova JY, Lakhter AJ, Loksh A, Yong WH, Riedinger MS, Miner JH, Sorokin LM, Ljubimov AV, and Black KL. Overexpression of α4 chain-containing laminins in human glial tumors identified by gene microarray analysis. Cancer Res 61: 5601-5610, 2001.
43. Lohikangas L, Gullberg D, and Johansson S. Assembly of laminin polymers is dependent on β1-integrins. Exp Cell Res 265: 135-144, 2005.
44. Maruyama Y. An electron microscopic study of circumferential mesangial interposition in various renal diseases. Nippon Jinzo Gakkai Shi 40: 263-275, 1998.
45. Matsuura H, Momota Y, Murata K, Matsushima H, Suzuki N, Nomizu M, Shinkai H, and Utani A. Localization of the laminin α4 chain in skin and identification of a heparin-dependent cell adhesion site within the laminin α4 chain C-terminal LG4 module. J Invest Dermatol 122: 614-620, 2004.
46. Miner JH. Developmental biology of glomerular basement membrane components. Curr Opin Nephrol Hypertens 7: 13-19, 1998.
47. Miner JH, Cong L, and Patton BL. Laminins α1 and α4 in pancreatic acinar basement membranes are required for basal receptor localization. J Histochem Cytochem 52: 153-156, 2005.
48. Miner JH and Li C. Defective glomerulogenesis in the absence of laminin alpha5 demonstrates a developmental role for the kidney glomerular basement membrane. Dev Biol 217: 278-289, 2000.
49. Nam TJ, Busby WH Jr, Rees C, and Clemmons DR. Thrombospondin and osteopontin bind to insulin-like growth factor (IGF)-binding protein-5 leading to an alteration in IGF-I-stimulated cell growth. Endocrinology 141: 1100-1106, 2000.
50. Nishiuchi R, Murayama O, Fujiwara H, Gu J, Kawakami T, Aimoto S, Wada Y, and Sekiguchi K. Characterization of the ligand-binding specificities of integrin α3β1 and α6β1 using a panel of purified laminin isoforms containing distinct α chains. J Biochem (Tokyo) 134: 497-504, 2003.
51. Noakes PG, Miner JH, Gautam M, Cunningham JM, Sanes JR, and Merlie JP. The renal glomerulus of mice lacking s-laminin/laminin β2: nephrosis despite molecular compensation by laminin β1. Nat Genet 10: 400-406, 1995.
52. Okazaki I, Suzuki N, Nishi N, Utani A, Matsuura H, Shinkai H, Yamashita H, Kitagawa Y, and Nomizu M. Identification of biologically active sequences in the laminin α4 chain G domain. J Biol Chem 277: 37070-37078, 2002.
53. Park IS, Kiyomoto H, Alvarez F, Xu YC, Abboud HE, and Abboud SL. Preferential expression of insulin-like growth factor binding proteins-1, -2, -5 during early diabetic renal hypertrophy in rats. Am J Kidney Dis 32: 1000-1010, 1998.
54. Parker A, Clarke JB, Busby WH Jr, and Clemmons DR. Identification of the extracellular matrix binding sites for insulin-like growth factor-binding protein 5. J Biol Chem 271: 13523-13529, 1996.
55. Patton BL, Cunningham JM, Thyboll J, Kortesmaa J, Westerblad H, Edstrom L, Tryggvason K, and Sanes JR. Properly formed but improperly localized synaptic specializations in the absences of laminin alpha4. Nat Neurosci 4: 597-604, 2001.
56. Pedraza C, Geberhiwot T, Ingerpuu S, Assefa D, Wondimu Z, Kortesmaa J, Tryggvason K, Virtanen I, and Patarroyo M. Monocytic cells synthesize, adhere to, and migrate on laminin-8 (α4β1γ1). J Immunol 165: 5831-5838, 2001.
57. Petäjäniemi N, Korhonen M, Kortesmaa J, Tryggvason K, Sekiguchi K, Fujiwara H, Sorokin L, Thornell LE, Wondimu Z, Assefa D, Patarroyo M, and Virtanen I. Localization of laminin α4-chain in developing and adult human tissues. J Histochem Cytochem 50: 1113-1130, 2002.
58. Ridley AJ, Schwartz MA, Burridge K, Firtel RA, Ginsberg MH, Borisy G, Parsons JT, and Horwitz AR. Cell migration: integrating signals from front to back. Science 302: 1704-1709, 2003.
59. Schneider MR, Wolf E, Hoeflich A, and Lahm H. IGF-binding protein-5: flexible player in the IGF system and effector on its own. J Endocrinol 172: 423-440, 2002.
60. St. John PL and Abrahamson DR. Glomerular endothelial cells and podocytes jointly synthesize laminin-1 and laminin-11 chains. Kidney Int 60: 1037-1046, 2001.
61. Talts JF, Sasaki T, Miosge N, Gohring W, Mann K, Mayne R, and Timpl R. Structural and functional analysis of the recombinant G domain of the laminin α4 chain and its proteolytic processing in tissues. J Biol Chem 275: 35192-35199, 2000.
62. Thyboll J, Kortesmaa J, Cao R, Soininen R, Wang L, Iivanainen A, Sorokin L, Risling M, Cao Y, and Tryggvason K. Deletion of the laminin α4 chain leads to impaired microvessel maturation. Mol Cell Biol 22: 1194-1202, 2002.
63. Wang J, Hoshijima M, Lam J, Zhou Z, Jokiel A, Dalton ND, Hultenby K, Ruiz-Lozano P, Ross J Jr, Tryggvason K, and Chien KR. Cardiomyopathy associated with microcirculation dysfunction in lamininα4 chain-deficient mice. J Biol Chem 281: 213-220, 2006.
64. Yamaguchi H, Yamashita H, Mori H, Okazaki I, Nomizu M, Beck K, and Kitagawa Y. High and low affinity heparin-binding sites in the G domain of the mouse laminin α4 chain. J Biol Chem 275: 29458-29465, 2000.
65. Yamashita H, Beck K, and Kitagawa Y. Heparin binds to the laminin α chain LG4 domain at a site different from that found for other laminins. J Mol Biol 335: 1145-1149, 2004.
66. Zenker M, Aigner T, Wendler O, Tralau T, Müntefering H, Fenski R, Pitz S, Schumacher V, Royer-Pokora B, Wühl E, Cochat P, Bouvier R, Kraus C, Mark K, Maldon H, Dötsch J, Rascher W, Maruniak-Chudek I, Lennert T, Neumann LM, and Reis A. Human laminin β2 deficiency causes congenital nephrosis with mesangial sclerosis and distinct eye abnormalities. Hum Mol Genet 2004.