Neutrophils are immune cells preferentially targeted by retinoic acid in elderly subjects

Immunity and Ageing

Volumn 7, Issue , 2010, Pages

  Minet Quinard, Régine ^a   Farges, M Chantal ^a   Thivat, Emilie ^a   Deleine, Cécile ^a   Mayot, Gilles ^a   Brtko, Julius ^b   Ribalta, Josep ^c   Winklhofer Roob, Brigitte ^d   Rock, Edmond ^e   Vasson, M Paule ^a,f  

^a CRNH AUVERGNE   (France)

^b INSTITUTE OF EXPERIMENTAL ENDOCRINOLOGY   (Slovakia)

^c INSTITUT D INVESTIGACIÓ SANITÀRIA PERE VIRGILI IISPV   (Spain)

^d UNIVERSITY OF GRAZ   (Austria)

^e CEMAGREF   (France)

^f CENTRE JEAN PERRIN   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; INTERLEUKIN 2; INTERLEUKIN RECEPTOR; RETINOIC ACID;

ADULT; ANTIGEN EXPRESSION; ARTICLE; BACTERICIDAL ACTIVITY; CD25+ T LYMPHOCYTE; CELL FUNCTION; CELL MIGRATION; CELL SURFACE; CYTOKINE PRODUCTION; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HUMAN; IMMUNE RESPONSE; MALE; NEUTROPHIL; NORMAL HUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PHAGOCYTOSIS; PHENOTYPE; POLYMORPHONUCLEAR CELL; PRIORITY JOURNAL;

EID: 77955669620     PISSN: 17424933     EISSN: None     Source Type: Journal    
DOI: 10.1186/1742-4933-7-10     Document Type: Article

References (87)

1. Aw D, Silva AB, Palmer DB. Immunosenescence: emerging challenges for an ageing population. Immunology 2007, 120:435-46. 10.1111/j.1365-2567.2007.02555.x, 2265901, 17313487.
2. Han S, Yang K, Ozen Z, Peng W, Marinova E, Kelsoe G, Zheng B. Enhanced differentiation of splenic plasma cells but diminished long-lived high-affinity bone marrow plasma cells in aged mice. J Immunol 2003, 170:1267-73.
3. Aspinall R. T cell development, ageing and Interleukin-7. Mech Ageing Dev 2006, 127:572-8. 10.1016/j.mad.2006.01.016, 16529797.
4. Panda A, Arjona A, Sapey E, Bai F, Fikrig E, Montgomery RR, Lord JM, Shaw AC. Human innate immunosenescence: causes and consequences for immunity in old age. Trends Immunol 2009, 30:325-33. 10.1016/j.it.2009.05.004, 19541535.
5. Gomez CR, Nomellini V, Faunce DE, Kovacs EJ. Innate immunity and aging. Exp Gerontol 2008, 43:718-28. 10.1016/j.exger.2008.05.016, 2564282, 18586079.
6. Lord JM, Butcher S, Killampali V, Lascelles D, Salmon M. Neutrophil ageing and immunesenescence. Mech Ageing Dev 2001, 122:1521-35. 10.1016/S0047-6374(01)00285-8, 11511394.
7. Crighton MH, Puppione AA. Geriatric neutrophils: implications for older adults. Semin Oncol Nurs 2006, 22:3-9. 10.1016/j.soncn.2005.10.002, 16458177.
8. Chatta GS, Andrews RG, Rodger E, Schrag M, Hammond WP, Dale DC. Hematopoietic progenitors and aging: alterations in granulocytic precursors and responsiveness to recombinant human G-CSF, GM-CSF, and IL-3. J Gerontol 1993, 48:M207-12.
9. Born J, Uthgenannt D, Dodt C, Nunninghoff D, Ringvolt E, Wagner T, Fehm HL. Cytokine production and lymphocyte subpopulations in aged humans. An assessment during nocturnal sleep. Mech Ageing Dev 1995, 84:113-26. 10.1016/0047-6374(95)01638-4, 8788239.
10. Chatta GS, Dale DC. Aging and haemopoiesis. Implications for treatment with haemopoietic growth factors. Drugs Aging 1996, 9:37-47. 10.2165/00002512-199609010-00004, 8818584.
11. MacGregor RR, Shalit M. Neutrophil function in healthy elderly subjects. J Gerontol 1990, 45:M55-60.
12. Tortorella C, Ottolenghi A, Pugliese P, Jirillo E, Antonaci S. Relationship between respiratory burst and adhesiveness capacity in elderly polymorphonuclear cells. Mech Ageing Dev 1993, 69:53-63. 10.1016/0047-6374(93)90071-X, 8397329.
13. Esparza B, Sanchez H, Ruiz M, Barranquero M, Sabino E, Merino F. Neutrophil function in elderly persons assessed by flow cytometry. Immunol Invest 1996, 25:185-90. 10.3109/08820139609059301, 9157053.
14. Biasi D, Carletto A, Dell'Agnola C, Caramaschi P, Montesanti F, Zavateri G, Zeminian S, Bellavite P, Bambara LM. Neutrophil migration, oxidative metabolism, and adhesion in elderly and young subjects. Inflammation 1996, 20:673-81. 10.1007/BF01488803, 8979154.
15. Corberand J, Ngyen F, Laharrague P, Fontanilles AM, Gleyzes B, Gyrard E, Senegas C. Polymorphonuclear functions and aging in humans. J Am Geriatr Soc 1981, 29:391-7.
16. Phair JP, Kauffman CA, Bjornson A, Gallagher J, Adams L, Hess EV. Host defenses in the aged: evaluation of components of the inflammatory and immune responses. J Infect Dis 1978, 138:67-73.
17. Chan SS, Monteiro HP, Deucher GP, Abud RL, Abuchalla D, Junqueira VB. Functional activity of blood polymorphonuclear leukocytes as an oxidative stress biomarker in human subjects. Free Radic Biol Med 1998, 24:1411-8. 10.1016/S0891-5849(98)00010-0, 9641258.
18. De Martinis M, Modesti M, Ginaldi L. Phenotypic and functional changes of circulating monocytes and polymorphonuclear leucocytes from elderly persons. Immunol Cell Biol 2004, 82:415-20. 10.1111/j.0818-9641.2004.01242.x, 15283852.
19. Damtew B, Spagnuolo PJ, Goldsmith GG, Marino JA. Neutrophil adhesion in the elderly: inhibitory effects of plasma from elderly patients. Clin Immunol Immunopathol 1990, 54:247-55. 10.1016/0090-1229(90)90086-6, 2295155.
20. Alonso-Fernandez P, Puerto M, Mate I, Ribera JM, de la Fuente M. Neutrophils of centenarians show function levels similar to those of young adults. J Am Geriatr Soc 2008, 56:2244-51. 10.1111/j.1532-5415.2008.02018.x, 19093924.
21. Niwa Y, Kasama T, Miyachi Y, Kanoh T. Neutrophil chemotaxis, phagocytosis and parameters of reactive oxygen species in human aging: cross-sectional and longitudinal studies. Life Sci 1989, 44:1655-64. 10.1016/0024-3205(89)90482-7, 2733545.
22. Polignano A, Tortorella C, Venezia A, Jirillo E, Antonaci S. Age-associated changes of neutrophil responsiveness in a human healthy elderly population. Cytobios 1994, 80:145-53.
23. Wenisch C, Patruta S, Daxbock F, Krause R, Horl W. Effect of age on human neutrophil function. J Leukoc Biol 2000, 67:40-5.
24. Izgut-Uysal VN, Agac A, Karadogan I, Derin N. Effects of L-carnitine on neutrophil functions in aged rats. Mech Ageing Dev 2003, 124:341-7. 10.1016/S0047-6374(03)00004-6, 12663132.
25. Mege JL, Capo C, Michel B, Gastaut JL, Bongrand P. Phagocytic cell function in aged subjects. Neurobiol Aging 1988, 9:217-20. 10.1016/S0197-4580(88)80054-X, 2836744.
26. Gocer P, Gurer US, Erten N, Palanduz S, Rayaman E, Akarsu B, Karan A, Cevikbas A. Comparison of polymorphonuclear leukocyte functions in elderly patients and healthy young volunteers. Med Princ Pract 2005, 14:382-5. 10.1159/000088109, 16220009.
27. Walrand S, Moreau K, Caldefie F, Tridon A, Chassagne J, Portefaix G, Cynober L, Beaufrere B, Vasson MP, Boirie Y. Specific and nonspecific immune responses to fasting and refeeding differ in healthy young adult and elderly persons. Am J Clin Nutr 2001, 74:670-8.
28. Rumore MM. Vitamin A as an immunomodulating agent. Clin Pharm 1993, 12:506-14.
29. Hanley TM, Kiefer HL, Schnitzler AC, Marcello JE, Viglianti GA. Retinoid-dependent restriction of human immunodeficiency virus type 1 replication in monocytes/macrophages. J Virol 2004, 78:2819-30. 10.1128/JVI.78.6.2819-2830.2004, 353720, 14990701.
30. Bjersing JL, Telemo E, Dahlgren U, Hanson LA. Loss of ileal IgA+ plasma cells and of CD4+ lymphocytes in ileal Peyer's patches of vitamin A deficient rats. Clin Exp Immunol 2002, 130:404-8. 10.1046/j.1365-2249.2002.02009.x, 1906545, 12452829.
31. Stephensen CB, Jiang X, Freytag T. Vitamin A deficiency increases the in vivo development of IL-10-positive Th2 cells and decreases development of Th1 cells in mice. J Nutr 2004, 134:2660-6.
32. Cui D, Moldoveanu Z, Stephensen CB. High-level dietary vitamin A enhances T-helper type 2 cytokine production and secretory immunoglobulin A response to influenza A virus infection in BALB/c mice. J Nutr 2000, 130:1132-9.
33. Semba RD. The role of vitamin A and related retinoids in immune function. Nutr Rev 1998, 56:S38-48. 10.1111/j.1753-4887.1998.tb01643.x, 9481123.
34. Stephensen CB. Vitamin A, infection, and immune function. Annu Rev Nutr 2001, 21:167-92. 10.1146/annurev.nutr.21.1.167, 11375434.
35. Villamor E, Fawzi WW. Effects of vitamin a supplementation on immune responses and correlation with clinical outcomes. Clin Microbiol Rev 2005, 18:446-64. 10.1128/CMR.18.3.446-464.2005, 1195969, 16020684.
36. Dzhagalov I, Chambon P, He YW. Regulation of CD8+ T lymphocyte effector function and macrophage inflammatory cytokine production by retinoic acid receptor gamma. J Immunol 2007, 178:2113-21.
37. Borel P, Mekki N, Boirie Y, Partier A, Alexandre-Gouabau MC, Grolier P, Beaufrere B, Portugal H, Lairon D, Azais-Braesco V. Comparison of the postprandial plasma vitamin A response in young and older adults. J Gerontol A Biol Sci Med Sci 1998, 53:B133-40.
38. Haller J, Weggemans RM, Lammi-Keefe CJ, Ferry M. Changes in the vitamin status of elderly Europeans: plasma vitamins A, E, B-6, B-12, folic acid and carotenoids. SENECA Investigators. Eur J Clin Nutr 1996, 50(Suppl 2):S32-46.
39. Szabova L, Macejova D, Dvorcakova M, Mostbock S, Blazickova S, Zorad S, Walrand S, Cardinault N, Vasson MP, Rock E, Brtko J. Expression of nuclear retinoic acid receptor in peripheral blood mononuclear cells (PBMC) of healthy subjects. Life Sci 2003, 72:831-6. 10.1016/S0024-3205(02)02307-X, 12479981.
40. Brtko J, Rock E, Nezbedova P, Krizanova O, Dvorcakova M, Minet-Quinard R, Farges MC, Ribalta J, Winklhofer-Roob BM, Vasson MP, Macejova D. Age-related change in the retinoid × receptor beta gene expression in peripheral blood mononuclear cells of healthy volunteers: effect of 13-cis retinoic acid supplementation. Mech Ageing Dev 2007, 128:594-600. 10.1016/j.mad.2007.08.005, 17916375.
41. Anlasik T, Sies H, Griffiths HR, Mecocci P, Stahl W, Polidori MC. Dietary habits are major determinants of the plasma antioxidant status in healthy elderly subjects. Br J Nutr 2005, 94:639-42. 10.1079/BJN20051574, 16277763.
42. Comstock GW, Menkes MS, Schober SE, Vuilleumier JP, Helsing KJ. Serum levels of retinol, beta-carotene, and alpha-tocopherol in older adults. Am J Epidemiol 1988, 127:114-23.
43. Hallfrisch J, Muller DC, Singh VN. Vitamin A and E intakes and plasma concentrations of retinol, beta-carotene, and alpha-tocopherol in men and women of the Baltimore Longitudinal Study of Aging. Am J Clin Nutr 1994, 60:176-82.
44. Helmer C, Peuchant E, Letenneur L, Bourdel-Marchasson I, Larrieu S, Dartigues JF, Dubourg L, Thomas MJ, Barberger-Gateau P. Association between antioxidant nutritional indicators and the incidence of dementia: results from the PAQUID prospective cohort study. Eur J Clin Nutr 2003, 57:1555-61. 10.1038/sj.ejcn.1601724, 14647220.
45. Hercberg S, Preziosi P, Galan P, Devanlay M, Keller H, Bourgeois C, Potier de Courcy G, Cherouvrier F. Vitamin status of a healthy French population: dietary intakes and biochemical markers. Int J Vitam Nutr Res 1994, 64:220-32.
46. Neale RJ, Lim H, Turner J, Freeman C, Kemm JR. The excretion of large vitamin C loads in young and elderly subjects: an ascorbic acid tolerance test. Age Ageing 1988, 17:35-41. 10.1093/ageing/17.1.35, 3364309.
47. Palli D, Decarli A, Russo A, Cipriani F, Giacosa A, Amadori D, Salkeld R, Salvini S, Buiatti E. Plasma levels of antioxidant vitamins and cholesterol in a large population sample in central-northern Italy. Eur J Nutr 1999, 38:90-8. 10.1007/s003940050049, 10352948.
48. Polito A, Intorre F, Andriollo-Sanchez M, Azzini E, Raguzzini A, Meunier N, Ducros V, O'Connor JM, Coudray C, Roussel AM, Maiani G. Estimation of intake and status of vitamin A, vitamin E and folate in older European adults: the ZENITH. Eur J Clin Nutr 2005, 59(Suppl 2):S42-7. 10.1038/sj.ejcn.1602297, 16254580.
49. Walston J, Xue Q, Semba RD, Ferrucci L, Cappola AR, Ricks M, Guralnik J, Fried LP. Serum antioxidants, inflammation, and total mortality in older women. Am J Epidemiol 2006, 163:18-26. 10.1093/aje/kwj007, 16306311.
50. Feart C, Siewe A, Samieri C, Peuchant E, Helmer C, Alfos S, Pallet V, Barberger-Gateau P. Plasma retinol and association with socio-demographic and dietary characteristics of free-living older persons: the bordeaux sample of the three-city study. Int J Vitam Nutr Res 2010, 80:32-44. 10.1024/0300-9831/a000004, 20533243.
51. Ligthart GJ, Corberand JX, Fournier C, Galanaud P, Hijmans W, Kennes B, Muller-Hermelink HK, Steinmann GG. Admission criteria for immunogerontological studies in man: the SENIEUR protocol. Mech Ageing Dev 1984, 28:47-55. 10.1016/0047-6374(84)90152-0, 6513613.
52. Wyss R, Bucheli F. Determination of endogenous levels of 13-cis-retinoic acid (isotretinoin), all-trans-retinoic acid (tretinoin) and their 4-oxo metabolites in human and animal plasma by high-performance liquid chromatography with automated column switching and ultraviolet detection. J Chromatogr B Biomed Sci Appl 1997, 700:31-47. 10.1016/S0378-4347(97)00303-4, 9390712.
53. Walrand S, Valeix S, Rodriguez C, Ligot P, Chassagne J, Vasson MP. Flow cytometry study of polymorphonuclear neutrophil oxidative burst: a comparison of three fluorescent probes. Clin Chim Acta 2003, 331:103-10. 10.1016/S0009-8981(03)00086-X, 12691870.
54. Lesourd B, Mazari L. Nutrition and immunity in the elderly. Proc Nutr Soc 1999, 58:685-95. 10.1079/PNS19990013, 10604204.
55. Engedal N, Ertesvag A, Blomhoff HK. Survival of activated human T lymphocytes is promoted by retinoic acid via induction of IL-2. Int Immunol 2004, 16:443-53. 10.1093/intimm/dxh048, 14978018.
56. Ertesvag A, Aasheim HC, Naderi S, Blomhoff HK. Vitamin A potentiates CpG-mediated memory B-cell proliferation and differentiation: involvement of early activation of p38MAPK. Blood 2007, 109:3865-72. 10.1182/blood-2006-09-046748, 17209053.
57. Haynes L, Eaton SM, Burns EM, Randall TD, Swain SL. Newly generated CD4 T cells in aged animals do not exhibit age-related defects in response to antigen. J Exp Med 2005, 201:845-51. 10.1084/jem.20041933, 2213095, 15781577.
58. Mittler JN, Lee WT. Antigen-specific CD4 T cell clonal expansion and differentiation in the aged lymphoid microenvironment. II. The memory T cell response is diminished. Mech Ageing Dev 2004, 125:59-68. 10.1016/j.mad.2003.10.003, 14706238.
59. Mittler JN, Lee WT. Antigen-specific CD4 T cell clonal expansion and differentiation in the aged lymphoid microenvironment. I. The primary T cell response is unaffected. Mech Ageing Dev 2004, 125:47-57. 10.1016/j.mad.2003.10.004, 14706237.
60. Eaton SM, Maue AC, Swain SL, Haynes L. Bone marrow precursor cells from aged mice generate CD4 T cells that function well in primary and memory responses. J Immunol 2008, 181:4825-31. 2582190, 18802086.
61. Cardinault N, Tyssandier V, Grolier P, Winklhofer-Roob BM, Ribalta J, Bouteloup-Demange C, Rock E, Borel P. Comparison of the postprandial chylomicron carotenoid responses in young and older subjects. Eur J Nutr 2003, 42:315-23. 10.1007/s00394-003-0426-2, 14673604.
62. McKerrow KJ, MacKie RM, Lesko MJ, Pearson C. The effect of oral retinoid therapy on the normal human immune system. Br J Dermatol 1988, 119:313-20. 10.1111/j.1365-2133.1988.tb03223.x, 2972309.
63. Prabhala RH, Maxey V, Hicks MJ, Watson RR. Enhancement of the expression of activation markers on human peripheral blood mononuclear cells by in vitro culture with retinoids and carotenoids. J Leukoc Biol 1989, 45:249-54.
64. Watson RR, Jackson JC, Alberts DS, Hicks MJ. Cellular immune functions of adults treated with a daily, long-term, low dose of 13-cis retinoic acid. J Leukoc Biol 1986, 39:567-77.
65. Prabhala RH, Garewal HS, Hicks MJ, Sampliner RE, Watson RR. The effects of 13-cis-retinoic acid and beta-carotene on cellular immunity in humans. Cancer 1991, 67:1556-60. 10.1002/1097-0142(19910315)67:6<1556::AID-CNCR2820670616>3.0.CO;2-O, 1825802.
66. Fortes C, Forastiere F, Agabiti N, Fano V, Pacifici R, Virgili F, Piras G, Guidi L, Bartoloni C, Tricerri A, Zuccaro P, Ebrahim S, Perucci CA. The effect of zinc and vitamin A supplementation on immune response in an older population. J Am Geriatr Soc 1998, 46:19-26.
67. Goto S, Okada N, Kaneko A, Isemura M. Different effects of all-trans-retinoic acid on phorbol ester-stimulated and phytohemagglutinin-stimulated interleukin-2 expression in human T-cell lymphoma HUT-78 cells. Cell Struct Funct 2008, 33:13-9. 10.1247/csf.07020, 18296860.
68. Ertesvag A, Austenaa LM, Carlsen H, Blomhoff R, Blomhoff HK. Retinoic acid inhibits in vivo interleukin-2 gene expression and T-cell activation in mice. Immunology 2009, 126:514-22. 10.1111/j.1365-2567.2008.02913.x, 2673363, 18778286.
69. Aukrust P, Muller F, Ueland T, Svardal AM, Berge RK, Froland SS. Decreased vitamin A levels in common variable immunodeficiency: vitamin A supplementation in vivo enhances immunoglobulin production and downregulates inflammatory responses. Eur J Clin Invest 2000, 30:252-9. 10.1046/j.1365-2362.2000.00619.x, 10692003.
70. Hoag KA, Nashold FE, Goverman J, Hayes CE. Retinoic acid enhances the T helper 2 cell development that is essential for robust antibody responses through its action on antigen-presenting cells. J Nutr 2002, 132:3736-9.
71. Stephensen CB, Rasooly R, Jiang X, Ceddia MA, Weaver CT, Chandraratna RA, Bucy RP. Vitamin A enhances in vitro Th2 development via retinoid × receptor pathway. J Immunol 2002, 168:4495-503.
72. Iwata M, Eshima Y, Kagechika H. Retinoic acids exert direct effects on T cells to suppress Th1 development and enhance Th2 development via retinoic acid receptors. Int Immunol 2003, 15:1017-25. 10.1093/intimm/dxg101, 12882839.
73. Ma Y, Chen Q, Ross AC. Retinoic acid and polyriboinosinic:polyribocytidylic acid stimulate robust anti-tetanus antibody production while differentially regulating type 1/type 2 cytokines and lymphocyte populations. J Immunol 2005, 174:7961-9.
74. Spilianakis CG, Lee GR, Flavell RA. Twisting the Th1/Th2 immune response via the retinoid × receptor: lessons from a genetic approach. Eur J Immunol 2005, 35:3400-4. 10.1002/eji.200535588, 16331704.
75. Stephensen CB, Borowsky AD, Lloyd KC. Disruption of Rxra gene in thymocytes and T lymphocytes modestly alters lymphocyte frequencies, proliferation, survival and T helper type 1/type 2 balance. Immunology 2007, 121:484-98. 10.1111/j.1365-2567.2007.02595.x, 2265968, 17433077.
76. Twining SS, Schulte DP, Wilson PM, Fish BL, Moulder JE. Vitamin A deficiency alters rat neutrophil function. J Nutr 1997, 127:558-65.
77. Hemila H, Wikstrom M. Retinoids activate superoxide production by polymorphonuclear leucocytes. Scand J Immunol 1985, 21:227-34. 10.1111/j.1365-3083.1985.tb01425.x, 2986277.
78. Badwey JA, Robinson JM, Curnutte JT, Karnovsky MJ, Karnovsky ML. Retinoids stimulate the release of superoxide by neutrophils and change their morphology. J Cell Physiol 1986, 127:223-8. 10.1002/jcp.1041270206, 3009496.
79. Lochner JE, Badwey JA, Horn W, Karnovsky ML. all-trans-Retinal stimulates superoxide release and phospholipase C activity in neutrophils without significantly blocking protein kinase C. Proc Natl Acad Sci USA 1986, 83:7673-7. 10.1073/pnas.83.20.7673, 386783, 3020554.
80. Eicher SD, Morrill JL, Blecha F. Vitamin concentration and function of leukocytes from dairy calves supplemented with vitamin A, vitamin E, and beta-carotene in vitro. J Dairy Sci 1994, 77:560-5. 10.3168/jds.S0022-0302(94)76984-8, 8182180.
81. Tjoelker LW, Chew BP, Tanaka TS, Daniel LR. Bovine Vitamin A and/3-Carotene Intake and Lactational Status. 1. Responsiveness of Peripheral Blood Polymorphonuclear Leukocytes to Vitamin A and/3-Carotene Challenge In Vitro. j dairy sci 1988, 71:3112-19. 10.3168/jds.S0022-0302(88)79911-7, 3230191.
82. Michal JJ, Heirman LR, Wongt S, Chew BP, Frigg M, Volker L. Modulatory effects of dietary, carotene on blood and mammary leukocyte function in periparturient dairy cows'. J Dairy Sci 1994, 77:1408-21. 10.3168/jds.S0022-0302(94)77079-X, 8046080.
83. Berton G, Lowell CA. Integrin signalling in neutrophils and macrophages. Cell Signal 1999, 11:621-35. 10.1016/S0898-6568(99)00003-0, 10530871.
84. Zouki C, Zhang SL, Chan JS, Filep JG. Peroxynitrite induces integrin-dependent adhesion of human neutrophils to endothelial cells via activation of the Raf-1/MEK/Erk pathway. Faseb J 2001, 15:25-27.
85. Fernandez-Patron C, Zouki C, Whittal R, Chan JS, Davidge ST, Filep JG. Matrix metalloproteinases regulate neutrophil-endothelial cell adhesion through generation of endothelin-1[1-32]. Faseb J 2001, 15:2230-40. 10.1096/fj.01-0178com, 11641250.
86. Clemens RA, Newbrough SA, Chung EY, Gheith S, Singer AL, Koretzky GA, Peterson EJ. PRAM-1 is required for optimal integrin-dependent neutrophil function. Mol Cell Biol 2004, 24:10923-32. 10.1128/MCB.24.24.10923-10932.2004, 533979, 15572693.
87. Walzog B, Weinmann P, Jeblonski F, Scharffetter-Kochanek K, Bommert K, Gaehtgens P. A role for beta(2) integrins (CD11/CD18) in the regulation of cytokine gene expression of polymorphonuclear neutrophils during the inflammatory response. Faseb J 1999, 13:1855-65.