N-terminal proteolytic processing by cathepsin G converts RANTES/CCL5 and related analogs into a truncated 4-68 variant

Journal of Leukocyte Biology

Volumn 80, Issue 6, 2006, Pages 1395-1404

  Lim, Jean K ^a,b   Lu, Wuyuan ^a   Hartley, Oliver ^c   DeVico, Anthony L ^a,d  

^a INSTITUTE OF HUMAN VIROLOGY   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

^d UNIVERSITY OF MARYLAND   (United States)

Author keywords

Antiviral; Chemokine; HIV; Microbicide; Neutrophils

Indexed keywords

CATHEPSIN G; CATHEPSIN G ANTIBODY; EGLIN C; ENZYME ANTIBODY; LEUKOCYTE ELASTASE; METHIONINE; RANTES;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN VARIANT; UTERINE CERVIX CYTOLOGY;

ANTIBODIES; ANTIVIRAL AGENTS; CATHEPSINS; CHEMOTAXIS; HIV INFECTIONS; HUMANS; NEUTROPHILS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEINS; RANTES; RECEPTORS, CCR5; RECOMBINANT PROTEINS; SERINE ENDOPEPTIDASES; SERINE PROTEINASE INHIBITORS;

EID: 33845418941     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0406290     Document Type: Article

References (92)

1. Zlotnik, A., Yoshie, O. (2000) Chemokines: a new classification system and their role in immunity. Immunity 12, 121-127.
2. Lau, E. K., Allen, S., Hsu, A. R., Handel, T. M. (2004) Chemokine-receptor interactions: GPCRs, glycosaminoglycans and viral chemokine binding proteins. Adv. Protein Chem. 68, 351-391.
3. Proudfoot, A. E., Handel, T. M., Johnson, Z., Lau, E. K., LiWang, P., Clark-Lewis, I., Borlat, F., Wells, T. N., and Kosco-Vilbois, M. H. (2003) Glycosaminoglycan binding and oligomerization are essential for the in vivo activity of certain chemokines. Proc Natl Acad Sci USA 100, 1885-1890
4. Jamieson, T., Cook, D. N., Nibbs, R. J., Rot, A., Nixon, C., McLean, P., Alcami, A., Lira, S. A., Wiekowski, M., Graham, G. J. (2005) The chemokine receptor D6 limits the inflammatory response in vivo. Nat. Immunol. 6, 403-411.
5. Locati, M., Torre, Y. M., Galliera, E., Bonecchi, R., Bodduluri, H., Vago, G., Vecchi, A., Mantovani, A. (2005) Silent chemoattractant receptors: D6 as a decoy and scavenger receptor for inflammatory CC chemokines. Cytokine Growth Factor Rev. 16, 679-686.
6. Martinez de la Torre, Y., Locati, M., Buracchi, C., Dupor, J., Cook, D. N., Bonecchi, R., Nebuloni, M., Rukavina, D., Vago, L., Vecchi, A., Lira, S. A., Mantovani, A. (2005) Increased inflammation in mice deficient for the chemokine decoy receptor D6. Eur J Immunol 35, 1342-1346
7. Delgado, M. B., Clark-Lewis, I., Loetscher, P., Langen, H., Thelen, M., Baggiolini, M., Wolf, M. (2001) Rapid inactivation of stromal cell-derived factor-1 by cathepsin G associated with lymphocytes. Eur. J. Immunol. 31, 699-707.
8. Detheux, M., Standker, L., Vakili, J., Munch, J., Forssmann, U., Adermann, K., Pohlmann, S., Vassart, G., Kirchhoff, F., Parmentier, M., et al. (2000) Natural proteolytic processing of hemofiltrate CC chemokine 1 generates a potent CC chemokine receptor (CCR)1 and CCR5 agonist with anti-HIV properties. J. Exp. Med. 192, 1501-1508.
9. Guan, E., Wang, J., Norcross, M. A. (2004) Amino-terminal processing of MIP-1beta/CCL4 by CD26/dipeptidyl-peptidase IV. J. Cell. Biochem. 92, 53-64.
10. Guan, E., Wang, J., Roderiquez, G., Norcross, M. A. (2002) Natural truncation of the chemokine MIP-1 beta /CCL4 affects receptor specificity but not anti-HIV-1 activity. J. Biol. Chem. 277, 32348-32352.
11. Lim, J. K., Burns, J. M., Lu, W., DeVico, A. L. (2005) Multiple pathways of amino terminal processing produce two truncated variants of RANTES/CCL5. J. Leukoc. Biol. 78, 442-452.
12. McQuibban, G. A., Gong, J. H., Tam, E. M., McCulloch, C. A., Clark-Lewis, I., Overall, C. M. (2000) Inflammation dampened by gelatinase A cleavage of monocyte chemoattractant protein-3. Science 289, 1202-1206.
13. McQuibban, G. A., Gong, J. H., Wong, J. P., Wallace, J. L., Clark-Lewis, I., Overall, C. M. (2002) Matrix metalloproteinase processing of monocyte chemoattractant proteins generates CC chemokine receptor antagonists with anti-inflammatory properties in vivo. Blood 100, 1160-1167.
14. Proost, P., Schutyser, E., Menten, P., Struyf, S., Wuyts, A., Opdenakker, G., Detheux, M., Parmentier, M., Durinx, C., Lambeir, A. M., et al. (2001) Amino-terminal truncation of CXCR3 agonists impairs receptor signaling and lymphocyte chemotaxis, while preserving antiangiogenic properties. Blood 98, 3554-3561.
15. Proost, P., Struyf, S., Schols, D., Opdenakker, G., Sozzani, S., Allavena, P., Mantovani, A., Augustyns, K., Bal, G., Haemers, A., et al. (1999) Truncation of macrophage-derived chemokine by CD26/ dipeptidyl-peptidase IV beyond its predicted cleavage site affects chemotactic activity and CC chemokine receptor 4 interaction. J. Biol. Chem. 274, 3988-3993.
16. Shioda, T., Kato, H., Ohnishi, Y., Tashiro, K., Ikegawa, M., Nakayama, E. E., Hu, H., Kato, A., Sakai, Y., Liu, H., et al. (1998) Anti-HIV-1 and chemotactic activities of human stromal cell-derived factor 1alpha (SDF-1alpha) and SDF-1beta are abolished by CD26/dipeptidyl peptidase IV-mediated cleavage. Proc. Natl. Acad. Sci. USA 95, 6331-6336.
17. Vakili, J., Standker, L., Detheux, M., Vassart, G., Forssmann, W. G., Parmentier, M. (2001) Urokinase plasminogen activator and plasmin efficiently convert hemofiltrate CC chemokine 1 into its active. J. Immunol. 167, 3406-3413.
18. Van den Steen, P. E., Proost, P., Wuyts, A., Van Damme, J., Opdenakker, G. (2000) Neutrophil gelatinase B potentiates interleukin-8 tenfold by aminoterminal processing, whereas it degrades CTAP-III, PF-4, and GRO-alpha and leaves RANTES and MCP-2 intact. Blood 96, 2673-2681.
19. Nufer, O., Corbett, M., Walz, A. (1999) Amino-terminal processing of chemokine ENA-78 regulates biological activity. Biochemistry 38, 636-642.
20. Ohashi, K., Naruto, M., Nakaki, T., Sano, E. (2003) Identification of interleukin-8 converting enzyme as cathepsin L. Biochim. Biophys. Acta 1649, 30-39.
21. Wolf, M., Clark-Lewis, I., Buri, C., Langen, H., Lis, M., Mazzucchelli, L. (2003) Cathepsin D specifically cleaves the chemokines macrophage inflammatory protein-1 alpha, macrophage inflammatory protein-1 beta, and SLC that are expressed in human breast cancer. Am. J. Pathol. 162, 1183-1190.
22. Leto, G., Tumminello, F. M., Crescimanno, M., Flandina, C., Gebbia, N. (2004) Cathepsin D expression levels in nongynecological solid tumors: clinical and therapeutic implications. Clin. Exp. Metastasis 21, 91-106.
23. Podgorski, I., Sloane, B. F. (2003) Cathepsin B and its role(s) in cancer progression. Biochem. Soc. Symp. 70, 263-276.
24. Sloane, B. F., Yan, S., Podgorski, I., Linebaugh, B. E., Cher, M. L., Mai, J., Cavallo-Medved, D., Sameni, M., Dosescu, J., Moin, K. (2005) Cathepsin B and tumor proteolysis: contribution of the tumor microenvironment. Semin. Cancer Biol. 15, 149-157.
25. Mishiro, T., Nakano, S., Takahara, S., Miki, M., Nakamura, Y., Yasuoka, S., Nikawa, T., Yasui, N. (2004) Relationship between cathepsin B and thrombin in rheumatoid arthritis. J. Rheumatol. 31, 1265-1273.
26. Taubert, H., Riemann, D., Kehlen, A., Meye, A., Bartel, F., John, V., Brandt, J., Bache, M., Wurl, P., Schmidt, H., et al. (2002) Expression of cathepsin B, D and L protein in juvenile idiopathic arthritis. Autoimmunity 35, 221-224.
27. Chaudhuri, A., Zbrzezna, V., Polyakova, J., Pogo, A. O., Hesselgesser, J., Horuk, R. (1994) Expression of the Duffy antigen in K562 cells. Evidence that it is the human erythrocyte chemokine receptor. J. Biol. Chem. 269, 7835-7838.
28. Horuk, R., Wang, Z. X., Peiper, S. C., Hesselgesser, J. (1994) Identification and characterization of a promiscuous chemokine-binding protein in a human erythroleukemic cell line. J. Biol. Chem. 269, 17730-17733.
29. Blanpain, C., Doranz, B. J., Vakili, J., Rucker, J., Govaerts, C., Baik, S. S., Lorthioir, O., Migeotte, I., Libert, F., Baleux, F., et al. (1999) Multiple charged and aromatic residues in CCR5 amino-terminal domain are involved in high affinity binding of both chemokines and HIV-1 Env protein. J. Biol. Chem. 274, 34719-34727.
30. Brandt, S. M., Mariani, R., Holland, A. U., Hope, T. J., Landau, N. R. (2002) Association of chemokine-mediated block to HIV entry with coreceptor internalization. J. Biol. Chem. 277, 17291-17299.
31. Lee, B., Sharron, M., Blanpain, C., Doranz, B. J., Vakili, J., Setoh, P., Berg, E., Liu, G., Guy, H. R., Durell, S. R., et al. (1999) Epitope mapping of CCR5 reveals multiple conformational states and distinct but overlapping structures involved in chemokine and coreceptor function. J. Biol. Chem. 274, 9617-9626.
32. Oravecz, T., Pall, M., Roderiquez, G., Gorrell, M. D., Ditto, M., Nguyen, N. Y., Boykins, R., Unsworth, E., Norcross, M. A. (1997) Regulation of the receptor specificity and function of the chemokine RANTES (regulated on activation, normal T cell expressed and secreted) by dipeptidyl peptidase IV (CD26)-mediated cleavage. J. Exp. Med. 186, 1865-1872.
33. Iwata, S., Yamaguchi, N., Munakata, Y., Ikushima, H., Lee, J. F., Hosono, O., Schlossman, S. F., Morimoto, C. (1999) CD26/dipeptidyl peptidase IV differentially regulates the chemotaxis of T cells and monocytes toward RANTES: possible mechanism for the switch from innate to acquired immune response. Int. Immunol. 11, 417-426.
34. Struyf, S., De Meester, I., Scharpe, S., Lenaerts, J. P., Menten, P., Wang, J. M., Proost, P., Van Damme, J. (1998) Natural truncation of RANTES abolishes signaling through the CC chemokine receptors CCR1 and CCR3, impairs its chemotactic potency and generates a CC chemokine inhibitor. Eur. J. Immunol. 28, 1262-1271.
35. Proost, P., De Meester, I., Schols, D., Struyf, S., Lambeir, A. M., Wuyts, A., Opdenakker, G., De Clercq, E., Scharpe, S., Van Damme, J. (1998) Amino-terminal truncation of chemokines by CD26/dipeptidyl-peptidase IV. Conversion of RANTES into a potent inhibitor of monocyte chemotaxis and HIV-1-infection. J. Biol. Chem. 273, 7222-7227.
36. Struyf, S., Proost, P., Schols, D., De Clercq, E., Opdenakker, G., Lenaerts, J. P., Detheux, M., Parmentier, M., De Meester, I., Scharpe, S., et al. (1999) CD26/dipeptidyl-peptidase IV down-regulates the eosinophil chemotactic potency, but not the anti-HIV activity of human eotaxin by affecting its interaction with CC chemokine receptor 3. J. Immunol. 162, 4903-4909.
37. Mack, M., Luckow, B., Nelson, P. J., Cihak, J., Simmons, G., Clapham, P. R., Signoret, N., Marsh, M., Stangassinger, M., Borlat, F., et al. (1998) Aminooxypentane-RANTES induces CCR5 internalization but inhibits recycling: a novel inhibitory mechanism of HIV infectivity. J. Exp. Med. 187, 1215-1224.
38. Hartley, O., Gaertner, H., Wilken, J., Thompson, D., Fish, R., Ramos, A., Pastore, C., Dufour, B., Cerini, F., Melotti, A., et al. (2004) Medicinal chemistry applied to a synthetic protein: development of highly potent HIV entry inhibitors. Proc. Natl. Acad. Sci. USA 101, 16460-16465.
39. Kawamura, T., Bruse, S. E., Abraha, A., Sugaya, M., Hartley, O., Offord, R. E., Arts, E. J., Zimmerman, P. A., Blauvelt, A. (2004) PSC-RANTES blocks R5 human immunodeficiency virus infection of Langerhans cells isolated from individuals with a variety of CCR5 diplotypes. J. Virol. 78, 7602-7609.
40. Proudfoot, A. E., Power, C. A., Hoogewerf, A. J., Montjovent, M. O., Borlat, F., Offord, R. E., Wells, T. N. (1996) Extension of recombinant human RANTES by the retention of the initiating methionine produces a potent antagonist. J. Biol. Chem. 271, 2599-2603.
41. Lederman, M. M., Veazey, R. S., Offord, R., Mosier, D. E., Dufour, J., Mefford, M., Piatak, M., Jr., Lifson, J. D., Salkowitz, J. R., Rodriguez, B., et al. (2004) Prevention of vaginal SHIV transmission in rhesus macaques through inhibition of CCR5. Science 306, 485-487.
42. Cauci, S., Guaschino, S., De Aloysio, D., Driussi, S., De Santo, D., Penacchioni, P., Quadrifoglio, F. (2003) Interrelationships of interleukin-8 with interleukin-1beta and neutrophils in vaginal fluid of healthy and bacterial vaginosis positive women. Mol. Hum. Reprod. 9, 53-58.
43. Panther, L. A., Tucker, L., Xu, C., Tuomala, R. E., Mullins, J. I., Anderson, D. J. (2000) Genital tract human immunodeficiency virus type 1 (HIV-1) shedding and inflammation and HIV-1 env diversity in perinatal HIV-1 transmission. J. Infect. Dis. 181, 555-563.
44. Thompson, L. A., Tomlinson, M. J., Barratt, C. L., Bolton, A. E., Cooke, I. D. (1991) Positive immunoselection - a method of isolating leukocytes from leukocytic reacted human cervical mucus samples. Am. J. Reprod. Immunol. 26, 58-61.
45. Wira, C. R., Fahey, J. V., Sentman, C. L., Pioli, P. A., Shen, L. (2005) Innate and adaptive immunity in female genital tract: cellular responses and interactions. Immunol. Rev. 206, 306-335.
46. Di Fabio, S., Corrias, F., Monardo, F., Titti, F. (2004) Flow cytometry analysis of immune cell populations isolated from cervicovaginal secretions of cynomolgus monkeys. J. Immunol. Methods 284, 7-14.
47. Levine, W. C., Pope, V., Bhoomkar, A., Tambe, P., Lewis, J. S., Zaidi, A. A., Farshy, C. E., Mitchell, S., Talkington, D. F. (1998) Increase in endocervical CD4 lymphocytes among women with nonulcerative sexually transmitted diseases. J. Infect. Dis. 177, 167-174.
48. Dewald, B., Rindler-Ludwig, R., Bretz, U., Baggiolini, M. (1975) Subcellular localization and heterogeneity of neutral proteases in neutrophilic polymorphonuclear leukocytes. J. Exp. Med. 141, 709-723.
49. Wiedow, O., Meyer-Hoffert, U. (2005) Neutrophil serine proteases: potential key regulators of cell signalling during inflammation. J. Intern. Med. 257, 319-328.
50. Campbell, E. J., Silverman, E. K., Campbell, M. A. (1989) Elastase and cathepsin G of human monocytes. Quantification of cellular content, release in response to stimuli, and heterogeneity in elastase-mediated proteolytic activity. J. Immunol. 143, 2961-2968.
51. Kargi, H. A., Campbell, E. J., Kuhn, C., III (1990) Elastase and cathepsin G of human monocytes: heterogeneity and subcellular localization to peroxidase-positive granules. J. Histochem. Cytochem. 38, 1179-1186.
52. Bae, Y. S., Bae, H., Kim, Y., Lee, T. G., Suh, P. G., Ryu, S. H. (2001) Identification of novel chemoattractant peptides for human leukocytes. Blood 97, 2854-2862.
53. Wilken, J., Hoover, D., Thompson, D. A., Barlow, P. N., McSparron, H., Picard, L., Wlodawer, A., Lubkowski, J., Kent, S. B. (1999) Total chemical synthesis and high-resolution crystal structure of the potent anti-HIV protein AOP-RANTES. Chem. Biol. 6, 43-51.
54. Lu, W., Randal, M., Kossiakoff, A., Kent, S. B. (1999) Probing intermolecular backbone H-bonding in serine proteinase-protein inhibitor complexes. Chem. Biol. 6, 419-427.
55. Lu, W. Y., Starovasnik, M. A., Dwyer, J. J., Kossiakoff, A. A., Kent, S. B., Lu, W. (2000) Deciphering the role of the electrostatic interactions involving Gly70 in eglin C by total chemical protein synthesis. Biochemistry 39, 3575-3584.
56. Ryu, O. H., Choi, S. J., Firatli, E., Choi, S. W., Hart, P. S., Shen, R. F., Wang, G., Wu, W. W., Hart, T. C. (2005) Proteolysis of macrophage inflammatory protein-1alpha isoforms LD78beta and LD78alpha by neutrophil-derived serine proteases. J. Biol. Chem. 280, 17415-17421.
57. Kameyoshi, Y., Dorschner, A., Mallet, A. I., Christophers, E., Schroder, J. M. (1992) Cytokine RANTES released by thrombin-stimulated platelets is a potent attractant for human eosinophils. J. Exp. Med. 176, 587-592.
58. Braun, N. J., Bodmer, J. L., Virca, G. D., Metz-Virca, G., Maschler, R., Bieth, J. G., Schnebli, H. P. (1987) Kinetic studies on the interaction of eglin c with human leukocyte elastase and cathepsin G. Biol. Chem. Hoppe Seyler 368, 299-308.
59. Okada, Y., Tsuboi, S., Tsuda, Y., Nakabayashi, K., Nagamatsu, Y., Yamamoto, J. (1989) Synthesis of peptide fragments related to eglin c and examination of their inhibitory effect on human leukocyte elastase, cathepsin G and alpha-chymotrypsin. Biochem. Biophys. Res. Commun. 161, 272-275.
60. Menendez-Arias, L., Risco, C., Oroszlan, S. (1992) Isolation and characterization of alpha 2-macroglobulin-protease complexes from purified mouse mammary tumor virus and culture supernatants from virus-infected cell lines. J. Biol. Chem. 267, 11392-11398.
61. Umezawa, H., Aoyagi, T., Okura, A., Morishima, H., Takeuchi, T. (1973) Letter: Elastatinal, a new elastase inhibitor produced by actinomycetes. J. Antibiot. (Tokyo) 26, 787-789.
62. Elsner, J., Mack, M., Bruhl, H., Dulkys, Y., Kimmig, D., Simmons, G., Clapham, P. R., Schlondorff, D., Kapp, A., Wells, T. N., et al. (2000) Differential activation of CC chemokine receptors by AOP-RANTES. J. Biol. Chem. 275, 7787-7794.
63. Proudfoot, A. E., Buser, R., Borlat, F., Alouani, S., Soler, D., Offord, R. E., Schroder, J. M., Power, C. A., Wells, T. N. (1999) Amino-terminally modified RANTES analogues demonstrate differential effects on RANTES receptors. J. Biol. Chem. 274, 32478-32485.
64. Matsui, M., Weaver, J., Proudfoot, A. E., Wujek, J. R., Wei, T., Richer, E., Trapp, B. D., Rao, A., Ransohoff, R. M. (2002) Treatment of experimental autoimmune encephalomyelitis with the chemokine receptor antagonist Met-RANTES. J. Neuroimmunol. 128, 16-22.
65. Chimura, T., Hirayama, T. (1993) Fluctuations in elastase of cervical mucus and clinical efficacy of cefodizime in obstetric and gynecologic infections. Jpn. J. Antibiot. 46, 730-735.
66. Nakai, A., Taniuchi, Y., Miyake, H., Nakai, M., Yokota, A., Takeshita, T. (2005) Increased level of granulocyte elastase in cervical secretion is an independent predictive factor for preterm delivery. Gynecol. Obstet. Invest. 60, 87-91.
67. El Messaoudi, K., Thiry, L., Van Tieghem, N., Liesnard, C., Englert, Y., Moguilevsky, N., Bollen, A. (1999) HIV-1 infectivity and host range modification by cathepsin D present in human vaginal secretions. AIDS 13, 333-339.
68. Milligan, G. N. (1999) Neutrophils aid in protection of the vaginal mucosae of immune mice against challenge with herpes simplex virus type 2. J. Virol. 73, 6380-6386.
69. Clark-Lewis, I., Kim, K. S., Rajarathnam, K., Gong, J. H., Dewald, B., Moser, B., Baggiolini, M., Sykes, B. D. (1995) Structure-activity relationships of chemokines. J. Leukoc. Biol. 57, 703-711.
70. Crump, M. P., Gong, J. H., Loetscher, P., Rajarathnam, K., Amara, A., Arenzana-Seisdedos, F., Virelizier, J. L., Baggiolini, M., Sykes, B. D., Clark-Lewis, I. (1997) Solution structure and basis for functional activity of stromal cell-derived factor-1; dissociation of CXCR4 activation from binding and inhibition of HIV-1. EMBO J. 16, 6996-7007.
71. Rajagopalan, L., Rajarathnam, K. (2004) Ligand selectivity and affinity of chemokine receptor CXCR1. Role of N-terminal domain. J. Biol. Chem. 279, 30000-30008.
72. Rajarathnam, K., Clark-Lewis, I., Sykes, B. D. (1994) 1H NMR studies of interleukin 8 analogs: characterization of the domains essential for function. Biochemistry 33, 6623-6630.
73. Wiedow, O., Muhle, K., Streit, V., Kameyoshi, Y. (1996) Human eosinophils lack human leukocyte elastase. Biochim. Biophys. Acta 1315, 185-187.
74. Bangalore, N., Travis, J. (1994) Comparison of properties of membrane-bound versus soluble forms of human leukocytic elastase and cathepsin G. Biol. Chem. Hoppe Seyler 375, 659-666.
75. Segal, A. W. (2005) How neutrophils kill microbes. Annu. Rev. Immunol. 23, 197-223.
76. Owen, C. A., Campbell, M. A., Boukedes, S. S., Campbell, E. J. (1995) Inducible binding of bioactive cathepsin G to the cell surface of neutrophils. A novel mechanism for mediating extracellular catalytic activity of cathepsin G. J. Immunol. 155, 5803-5810.
77. Owen, C. A., Campbell, M. A., Boukedes, S. S., Campbell, E. J. (1994) Monocytes recruited to sites of inflammation express a distinctive proinflammatory (P) phenotype. Am. J. Physiol. 267, L786-L796.
78. Owen, C. A., Campbell, M. A., Sannes, P. L., Boukedes, S. S., Campbell, E. J. (1995) Cell surface-bound elastase and cathepsin G on human neutrophils: a novel, non-oxidative mechanism by which neutrophils focus and preserve catalytic activity of serine proteinases. J. Cell Biol. 131, 775-789.
79. Padrines, M., Wolf, M., Walz, A., Baggiolini, M. (1994) Interleukin-8 processing by neutrophil elastase, cathepsin G and proteinase-3. FEBS Lett. 352, 231-235.
80. Polanowska, J., Krokoszynska, I., Czapinska, H., Watorek, W., Dadlez, M., Otlewski, J. (1998) Specificity of human cathepsin G. Biochim. Biophys. Acta 1386, 189-198.
81. Alkhatib, G., Combadiere, C., Broder, C. C., Feng, Y., Kennedy, P. E., Murphy, P. M., Berger, E. A. (1996) CC CKR5: a RANTES, MIP-1alpha, MIP-1beta receptor as a fusion cofactor for macrophage-tropic HIV-1. Science 272, 1955-1958.
82. Cocchi, F., DeVico, A. L., Garzino-Demo, A., Arya, S. K., Gallo, R. C., Lusso, P. (1995) Identification of RANTES, MIP-1 alpha, and MIP-1 beta as the major HIV-suppressive factors produced by CD8+ T cells. Science 270, 1811-1815.
83. Ahmed, R. K., Nilsson, C., Biberfeld, G., Thorstensson, R. (2001) Role of CD8+ cell-produced anti-viral factors in protective immunity in HIV-2-exposed but seronegative macaques resistant to intrarectal SIVsm challenge. Scand. J. Immunol. 53, 245-253.
84. Bergmeier, L. A., Wang, Y., Lehner, T. (2002) The role of immunity in protection from mucosal SIV infection in macaques. Oral Dis. 8, Suppl 2, 63-68.
85. Darville, T., Andrews, C. W., Jr., Sikes, J. D., Fraley, P. L., Rank, R. G. (2001) Early local cytokine profiles in strains of mice with different outcomes from chlamydial genital tract infection. Infect. Immun. 69, 3556-3561.
86. Fenyo, E. M. (1994) Antigenic variation of primate lentiviruses in humans and experimentally infected macaques. Immunol. Rev. 140, 131-146.
87. Gardner, M. (1991) SIV vaccines: current status. The role of the SIV-macaque model in AIDS research. Vaccine 9, 787-791.
88. Miller, C. J. (1998) Localization of Simian immunodeficiency virus-infected cells in the genital tract of male and female Rhesus macaques. J. Reprod. Immunol. 41, 331-339.
89. Al-Harthi, L., Kovacs, A., Coombs, R. W., Reichelderfer, P. S., Wright, D. J., Cohen, M. H., Cohn, J., Cu-Uvin, S., Watts, H., Lewis, S., et al. (2001) A menstrual cycle pattern for cytokine levels exists in HIV-positive women: implication for HIV vaginal and plasma shedding. AIDS 15, 1535-1543.
90. Belec, L., Ghys, P. D., Hocini, H., Nkengasong, J. N., Tranchot-Diallo, J., Diallo, M. O., Ettiegne-Traore, V., Maurice, C., Becquart, P., Matta, M., et al. (2001) Cervicovaginal secretory antibodies to human immunodeficiency virus type 1 (HIV-1) that block viral transcytosis through tight epithelial barriers in highly exposed HIV-1-seronegative African women. J. Infect. Dis. 184, 1412-1422.
91. Spear, G. T., Sha, B. E., Saarloos, M. N., Benson, C. A., Rydman, R., Massad, L. S., Gilmore, R., Landay, A. L. (1998) Chemokines are present in the genital tract of HIV-seropositive and HIV-seronegative women: correlation with other immune mediators. J. Acquir. Immune Defic. Syndr. Hum. Retrovirol. 18, 454-459.
92. Iqbal, S. M., Ball, T. B., Kimani, J., Kiama, P., Thottingal, P., Embree, J. E., Fowke, K. R., Plummer, F. A. (2005) Elevated T cell counts and RANTES expression in the genital mucosa of HIV-1-resistant Kenyan commercial sex workers. J. Infect. Dis. 192, 728-738.