Role of cyclic GMP signaling in the melanocyte response to hypergravity

Signal Transduction

Volumn 6, Issue 6, 2006, Pages 406-413

  Ivanova, Krassimira ^a   Block, Ingrid ^a   Das, Pranab K ^b   Gerzer, Rupert ^a  

^a GERMAN AEROSPACE CENTER DLR   (Germany)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

cGMP efflux; Hypergravity; Melanin; Melanocytes; Melanoma cell lines

Indexed keywords

CYCLIC GMP; GUANYLATE CYCLASE; MELANIN;

CELL FUNCTION; COSMONAUT; GRAVITY; HUMAN; MELANOCYTE; MELANOMA; PIGMENT DISORDER; PRIORITY JOURNAL; REVIEW; SKIN CANCER; SPACE FLIGHT;

EQUIDAE;

EID: 33845928289     PISSN: 16154053     EISSN: 16154061     Source Type: Journal    
DOI: 10.1002/sita.200600102     Document Type: Review

References (92)

1. Lucas, K.A., Pitari, G.M., Kazerounian, S., Ruiz-Stewart, I., Park, J., Schulz, S., Chepenik, K.P., Waldman, S.A. (2000) Guanylyl cyclases and signaling by cyclic GMP. Pharmacol. Res. 52: 375-413.
2. Garbers, D.L., Lowe, D.C. (1994) Guanylyl cyclase receptors. J. Biol. Chem. 269: 30741-30744.
3. Kuhn, M. (2003) Structure, regulation, and function of mammalian membrane guanylyl cyclase receptors, with a focus on guanylyl cyclaseA. Circ. Res. 93: 700-709.
4. Lewicki, JA., Potter, A.A. (1995): Physiological studies on natriuretic peptide family. In Hypertension: Pathophysiology, Diagnosis, and Management. Eds. Laragh, J.H., Brenner, B.M., Raven Press, New York (USA), pp. 1029-1053.
5. Forte, Jr., L.R. (2004) Uroguanylin and guanylin peptides: Pharmacology and experimental therapeutics. Pharmacol. Therapeut. 104: 137-162.
6. Cohen, M.B., Hawkins, J.A., Witte, D.P. (1998) Guanylin mRNA expression in human intestine and colorectal adenocarcinoma. Lab. Invest. 78: 101-108.
7. Waldman, S.A., Cagir, B., Rakinic, J., Fry, R.D., Goldstein, S.D., Isenberg, G., Barber, B.S., Biswas, M.S., Minimo, C., Palazzo, M.D., Park, P.K., Weinberg, D. (1998) Use of guanylyl cyclase C for detecting micrometastasis in lymph nodes of patients with colon cancer. Dis. Colon Rectum 41: 310-315.
8. Ivanova, K., Das, P.K., van den Wijngaard, R.M.J.G.J., Lenz, W., Klockenbring, T., Malcharzyk, V., Drummer, C., Gerzer, R. (2001) Differential expression of functional guanylyl cyclases in melanocytes: Absence of nitric oxide-sensitive isoform in metastatic cells. J. Invest. Dermatol. 116: 409-416.
9. Schmidt, H.H., Walter, U. (1994) NO at work. Cell 78: 919-925.
10. Bogdan, C. (2001) Nitric oxide and the immune response. Nat. Immunol. 2: 907-916.
11. Cals-Grierson, M.M., Ormerod, A.D. (2004) Nitric oxide function in the skin. Nitric Oxide 10: 179-193.
12. Ekmekcioglu, S., Tang, C.H., Grimm, E.A. (2005) NO news is not necessarily good news in cancer. Curr. Cancer Drug Targets 5: 103-115.
13. Gong, L., Pitari, G.M., Schulz, A., Waldman, S.A. (2004) Nitric oxide signaling: Systems integration of oxygen balance in defense of cell integrity. Curr. Opin. Hematol. 11: 7-14.
14. Ivanova, K., Le Poole, I.C., Gerzer, R., Westerhof, W., Das, P. (1997) Effects of nitric oxide on the adhesion of melanocytes to extracellular matrix components. J. Pathol. 183: 469-476.
15. Monteiro, H.P., Silva, E.F., Stern, A. (2004) Nitric oxide: A potential inducer of adhesion-related apoptosis - anoikis. Nitric Oxide 10: 1-10.
16. Ivanova, K., van den Wijngaard, R.M.J.G.J., Gerzer, R., Lamers, W.H., Das, P.K. (2005) Non-lesional vitiliginous melanocytes are not characterized by an increased proneness to nitric oxide-induced apoptosis. Exp. Dermatol. 14: 445-453.
17. Gerzer, R., Bohme, E., Hofmann, F., Schultz, G. (1981) Soluble guanylate cyclase purified from bovine lung contains heme and copper. FEBS Lett. 132: 71-74.
18. Ignarro, L.J. (1990) Haem-dependent activation of guanylate cyclase and cyclic GMP formation by endogenous nitric oxide: A unique transduction mechanism for transcellular signaling. Pharmacol. Toxicol. 67: 1-7.
19. Friebe, A., Koesling, D. (2003) Regulation of nitric oxide-sensitive guanylyl cyclase. Circ. Res. 93: 96-105.
20. 1-subunit yields a nitric oxide-sensitive form of soluble guanylyl cyclase. Proc. Natl. Acad. Sci. USA 91: 2592-2596.
21. Zhao, Y., Schelvis, J.P., Babcock, G.T., Marietta, M.A. (1998) Identification of histidine 105 in the beta1 subunit of soluble guanylate cyclase as the heme proximal ligand. Biochemistry 37: 4502-4509.
22. Schmidt, P.M., Schramm, M., Schröder, H., Wunder, F., Stasch, J.P. (2004) Identification of residues crucially involved in the binding of the heme moiety of soluble guanylate cyclase. J. Biol. Chem. 279: 3025-3032.
23. Pellicena, P., Karow, D.S., Boon, E.M., Marletta, MA., Kuriyan, J. (2004) Crystal structure of an oxygen-binding heme domain related to soluble guanylate cyclases. Proc. Natl. Acad. Sci. USA 101: 12854-12859.
24. Nioche, P., Berka, V., Vipond, J., Minton, N., Tsai, A.L., Raman, C.S. (2004) Femtomolar sensitivity of a NO sensor from Clostridium botulinum. Science 306: 1550-1553.
25. Boon, E.M., Marietta, M.A. (2005) Ligand discrimination in soluble guanylate cyclase and the HNOX family of heme sensor proteins. Curr. Opin. Chem. Biol. 9: 441-446.
26. Cary, S.P.L., Winger, J.A., Derbyshire, E.R., Marietta, S. (2006) Nitric oxide signaling: No longer simply on or off. Trends Biochem. Sci. 32: 231-239.
27. Stasch, J.P., Becker, E.M., Alonso-Alija, C., Apeler, H., Dembowsky, K., Feurer, A., Gerzer, R., Minuth, T., Perzborn, E., Plei, U., Schröder, H., Schroeder, W., Stahl, E., Steinke, W., Straub, A., Schramm, M. (2001) NO-independent regulatory site on soluble guanylate cyclase. Nature 410: 212-215.
28. Evgenov, O.V., Pacher, P., Schmidt, P.M., Haskó, G., Schmidt, H.H.H.W., Stasch, J.P. (2006) NO-independent stimulators and activators of soluble guanylate cyclase: Discovery and therapeutic potential. Nat. Rev. Drug Discov. 5: 755-768.
29. Schindler, U., Strobel, H., Schonafinger, K., Linz, W., Lohn, M., Martorana, P.A., Rutten, H., Schindler, P.W., Busch, A.E., Sohn, M., Topfer, A., Pistorius, A., Jannek, C., Mulsch, A. (2006) Biochemistry and pharmacology of novel anthranilic acid derivatives activating heme-oxidized soluble guanylyl cyclase. Mol. Pharmacol. 69: 1260-1268.
30. Feu, R., Kemp-Harper, B. (2006) cGMP signaling: From bench to bedside. EMBO Reports 7: 149-153.
31. Doggell, S. (2005) Clinical potential of nitric oxide-independent soluble guanylyl cyclase activators. Curr. Opin. Invest. Drugs 6: 874-878.
32. Hofmann, F. (2005) The biology of cyclic GMP-dependent protein kinases. J. Biol. Chem. 280: 1-4.
33. Sonderling, S.H., Beavo, J.A. (2000) Regulation of cAMP and cGMP signaling: New phosphodiesterases and new functions. Curr. Opin. Cell Biol. 12: 174-179.
34. Ludwig, A., Zong, X., Jeglitsch, M., Hofmann, F., Biel, M. (1998) A family of hyperpolarization-activated mammalian cation channels. Nature 393: 587-591.
35. Corbin, J.D., Francis, S.H. (1999) Cyclic GMP phosphodiesterase-5: Target of sildenafil. J. Biol. Chem. 274: 13729-13732.
36. Beavo, J.A., Brunton, L.L. (2002) Cyclic nucleotide research - still expanding after half a century. Nat. Rev. Mol. Cell Biol. 3: 710-718.
37. Pilz, R.B., Casteel, D.E. (2003) Regulation of gene expression by cyclic GMP. Circ. Res. 93: 1034-1046.
38. Jedlitschky, G., Burchell, B., Keppler, D. (2000) The multidrug resistance protein 5 functions as an ATP-dependent export pump for cyclic nucleotides. J. Biol. Chem. 275: 30069-30074.
39. Lai, L., Tan, T.M. (2002) Role of glutathione in the multidrug resistance protein 4 (MRP4/ABCC4)-mediated efflux of cAMP and resistance to purine analogues. Biochem. J. 361: 497-503.
40. van Aubel, R.A., Smeets, P.H., Peters, J.G., Bindels, R.J., Russel, F.G. (2002) The MRP4/ABCC4 gene encodes a novel apical organic anion transporter in human kidney proximal tubules: Putative efflux pump for urinary cAMP and cGMP. J. Am. Soc. Nephrol. 13: 595-603.
41. Thompson, W.J., Piazza, G.A., Li, H., Liu, L., Fetter, J., Zhu, B., Sperl, G., Ahnen, D., Pamukcu, R. (2000) Exisulind induction of apoptosis involves guanosine 3′,5′-cyclic monophosphate phosphodiesterase inhibition, protein kinase G activation, and attenuated beta-catenin. Cancer Res. 60: 3338-3342.
42. Sarfati, M., Mateo, V., Baudet, S., Rubio, M., Fernandez, C., Davi, F., Binet, J.L., Delic, J., Merle-Beral, H. (2003) Sildenafil and vardenafil, types 5 and 6 phosphodiesterase inhibitors, induce caspase-dependent apoptosis of B-chronic lymphocytic leukemia cells. Blood 101: 265-269.
43. Sundkvist, E., Jaeger, R., Sager, G. (2000) Leukotriene C(4) (LTC(4)) does not share a cellular efflux mechanism with cGMP: Characterization of cGMP transport by uptake to inside-out vesicles from human erythrocytes. Biochim. Biophys. Acta 1462: 121-130.
44. Li, Y., Maher, P., Schubert, D. (1997) Requirement for cGMP in nerve cell death caused by glutathione depletion. J. Cell Biol. 139: 1317-1324.
45. Montoliu, C., Llansola, M., Kosenko, E., Corbalan, R., Felipo, V. (1999) Role of cyclic GMP in glutamate neurotoxicity in primary cultures of cerebellar neurons. Neuropharmacology 38: 1883-1891.
46. + exchanger variant in cultured rat astrocytes via an extracellular site of action. J. Neurochem. 68: 1451-1461.
47. Poulopoulou, C., Nowak, L.M. (1998) Extracellular 3′,5′ cyclic guanosine monophosphate inhibits kainite-activated responses in cultured mouse cerebellar neurons. J. Pharmacol. Exp. Ther. 286: 99-109.
48. Kadekaro, A.L., Kavanagh, R.J., Wakamatsu, K., Ito, S., Pipitone, M.A., Abdel-Malek, Z.A. (2003) Cutaneous photobiology. The melanocyte vs. the sun: Who will win the final round? Pigment Cell Res. 16: 434-447.
49. Leiter, U., Meier, F., Schittek, B., Garbe, K. (2004) The natural course of cutaneous melanoma. J. Surg. Oncol. 86: 172-178.
50. Kollias, N., Sayre, R.M., Zeise, L., Chedekel, M.R. (1991) Photoprotection by melanin. J. Photochem. Photobiol. B 9: 135-160.
51. Kobayashi, N., Nakagawa, A., Muramatsu, T., Yamashina, Y., Shirai, T., Hashimoto, M.W., Ishigaki, Y., Ohnishi, T., Mori, T. (1998) Supranuclear melanin caps reduce ultraviolet induced DNA photoproducts in human epidermis. J. Invest. Dermatol. 110: 806-810.
52. Takeuchi, S., Zhang, W., Wakamatsu, K., Ito, S., Hearing, V.J., Kraemer, K.H., Brash, D.E. (2004) Melanin acts as a potent UVB photosensitizer to cause an atypical mode of cell death in murine skin. Proc. Natl. Acad. Sci. USA 101: 15076-15081.
53. Chedekel, M.R., Smith, S.K., Post, P.W., Pokora, A., Vessell, D.L. (1978) Photodestruction of pheomelanin: Role of oxygen. Proc. Natl. Acad. Sci. USA 75: 5395-5399.
54. Swartz, H.M., Sarna, T., Zecca, L. (1992) Modulation by neuromelanin of the availability and reactivity of metal ions. Ann. Neurol. 32: S69-S75.
55. Riley, P.A. (2003) Melanogenesis and melanoma. Pigment Cell Res. 16: 548-552.
56. Halaban, R. (2000) The regulation of normal melanocyte proliferation. Pigment Cell Res. 13: 4-14.
57. Park, H.Y., Gilchrest, B.A. (1999) Signaling pathways mediating melanogenesis. Cell Mol. Biol. 45: 919-930.
58. Emir, U.E., Kurnaz, I.A. (2003) An integrated model for melanocyte-specific gene expression and melanogenesis. Signal Transduction 3: 209-217.
59. Busca, R., Ballotti, R. (2000) Cyclic AMP a key messenger in the regulation of skin pigmentation. Pigment Cell Res. 13: 60-69.
60. Romero-Graillet, C., Aberdam, E., Biagioli, N., Massabni, W., Ortonne, J.P., Ballotti, R. (1996) Ultraviolet B radiation acts through the nitric oxide and cGMP signal transduction pathway to stimulate melanogenesis in human melanocytes. J. Biol. Chem. 271: 28052-28056.
61. Sasaki, M., Horikoshi, T., Uchiwa, H., Miyachi, Y. (2000) Up-regulation of tyrosinase gene by nitric oxide in human melanocytes. Pigment Cell Res. 13: 248-252.
62. Das, P.K., van den Wijngaard, R.M., Wankowicz-Kalinska, A., Le Poole, I.C. (2001) A symbiotic concept of autoimmunity and tumour immunity: Lessons from vitiligo. Trends Immunol. 22: 130-136.
63. Le Poole, I.C., Mutis, T., van den Wijngaard, R.M.J.G.J., Westerhof, W., Ottenhoff, T., Vries, R.R.P., Das, P.K. (1993) A novel, antigen-presenting function of melanocytes and its possible relationship to hypopigmentary disorders. J. Immunol. 151: 7284-7292.
64. Wankowicz-Kalinska, A., Le Poole, C., van den Wijngaard, R., Storkus, W.J., Das, P.K. (2003) Melanocyte-specific immune response in melanoma and vitiligo: Two faces of the same coin? Pigment Cell Res. 16: 254-260.
65. Chin, L. (2003) The genetics of malignant melanoma: Lessons from mouse and man. Nat. Rev. Cancer 3: 559-570.
66. Walker, G.J., Hayward, N.K. (2002) Pathways to melanoma development: Lesson from the mouse. J. Invest. Dermatol. 119: 783-792.
67. Herlyn, R. (2005) Metastatic melanoma cells. Introduction. Cancer Metastasis Rev. 24: 193-194.
68. Whiteman, D., Whiteman, C., Green, A. (2001) Childhood sun exposure as a risk factor for melanoma: A systematic review of epidemiologic studies. Cancer Causes Control 12: 69-82.
69. Miller, A.L., Mihm, Jr., M.C. (2006) Mechanisms of disease melanoma. N. Engl. J. Med. 355: 51-65.
70. Gottesman, M.M., Fojo, T., Bates, S.E. (2002) Multidrug resistance in cancer: Role of ATP-dependent transporters. Nat. Rev. Cancer 2: 48-58.
71. Serone, L., Hersey, P. (1999) The chemoresistance of human malignant melanoma: An update. Melanoma Res. 9: 51-58.
72. Helmbach, H., Sinha, P., Schadendorf, D. (2003) Human melanoma: Drug resistance. Recent Results Cancer Res. 16: 93-110.
73. Tang, C.H., Grimm, E.A. (2004) Depletion of endogeneous nitric oxide enhances cisplatin-induced apoptosis in a p53-dependent manner in melanoma cell lines. J. Biol. Chem. 279: 288-289.
74. Smalley, K.S., Haas, N.K., Bradford, P.A., Lioni, M., Flaherty, K.T., Herlyn, M. (2006) Multiple signaling pathways must be targeted to overcome drug resistance in cell lines derived from melanoma metastasis. Mol. Cancer Ther. 5: 1136-1144.
75. Alexandresku, D., Dutcher, J.P., Wiernik, P.H. (2005) Metastatic melanoma. Is biochemotherapy the future? Med. Oncol. 22: 101-111.
76. Herlyn, M. (2005) Molecular targets in melanoma: Strategies and challenges for diagnosis and therapy. Int. J. Cancer 118: 523-527.
77. de Groot, R.P., Rijken, P.J., den Hertog, J., Boonstra, J., Verkleij, A.J., de Laat, S.W., Kruijer, W. (1990) Microgravity decreases cfos induction and serum response element activity. J. Cell Sci. 97: 33-38.
78. de Groot, R.P., Rijken, P.J., den Hertog, J., Boonstra, J., Verkleij, A.J., de Laat, S.W., Kruijer, W. (1991) Nuclear responses to protein kinase C signal transduction are sensitive to gravity changes. Exp. Cell Res. 197: 87-90.
79. Kawashima, K., Shibata, R., Negishi, Y., Endo, H. (1998) Stimulative effect of high-level hypergravity on differentiated functions of osteoblast-like cells. Cell Struct. Funct. 23: 221-229.
80. Carmeliet, G., Bouillon, R. (1999) The effect of microgravity on morphology and gene expression of osteoblasts in vitro. FASEB J. 13: S129-S134.
81. Furutsu, M., Kawashima, K., Negishi, Y., Endo, H. (2000) Bidirectional effects of hypergravity on the cell growth and differentiated functions of osteoblast-like ROS17/2.8 cells. Biol. Pharm. Bull. 23: 1258-1261.
82. Takemura, M., Yoshida, S. (2001) Stimulation of DNA polymerase α by hypergravity generated by centrifugal acceleration. Biochem. Biophys. Res. Commun. 289: 345-349.
83. Bernd, A., Ramirez-Boska, A., Görmar, F.E., Bereiter-Hahn, J., Holzmann, H. (1992) UVA/B and mechanical pressure induce melanin formation by human melanocytes in culture. Eur. J. Dermatol. 2: 450-451.
84. Kippenberger, S., Bernd, A., Loitsch, S., Muller, J., Guschel, M., Kaufmann, R. (1999) Cyclic stretch up-regulates proliferation and heat shock protein 90 expression in human melanocytes. Pigment Cell Res. 12: 246-251.
85. Kippenberger, S., Loitsch, S., Muller, J., Guschel, M., Ramirez-Bosca, A., Kaufmann, R., Bernd, A. (2000) Melanocytes respond to mechanical stretch by activation of mitogen-activated protein kinases (MAPK). Pigment Cell Res. 13: 278-280.
86. Gauthier, Y., Cario-Andre, M., Lepreux, S., Pain, C., Taieb, A. (2003) Melanocyte detachment after skin friction in non lesional skin with generalized vitiligo. Br. J. Dermatol. 148: 95-101.
87. Le Poole, I.C., Sarangarajan, R., Zhao, Y., Stennett, L.S., Brown, T.L., Sheth, P., Miki, T., Boisy, R.E. (2001) ,VIT1', a novel gene associated with vitiligo. Pigment Cell Res. 14: 475-484.
88. Ivanova, K., Zadeh, N.H., Block, I., Das, P.K., Gerzer, R. (2004) Stimulation of cyclic GMP efflux in human melanocytes by hypergravity generated by centrifugal acceleration. Pigment Cell Res. 17: 471-479.
89. Stieber, C., Ivanova, K., Block, I., Gerzer, R. (2005) Hypergravity modulates cyclic GMP efflux in nitric oxide-stimulated human melanocytic cells. J. Gravit. Physiol. 12: 251-252.
90. Castro, L.R.V., Verde, I., Cooper, D.M., Fischmeister, R. (2006) Cyclic guanosine monophosphate compartmentation in rat cardiac myocytes. Circulation 113: 221-228.
91. Wielinga, P.R., van der Heijden, I., Reid, G., Beijnen, J.H., Wijnholds, J., Borst, P. (2003) Characterization of the MRP4- and MRP5-mediated transport of cyclic nucleotides from intact cells. J. Biol. Chem. 278: 17664-17671.
92. Ivanova, K., Lambers, B., Block, I., Bromeis, B., Das, P.K., Gerzer, R. (2005) Molecular mechanisms of gravity-dependent signaling in human melanocytic cells involve cyclic GMP. J. Gravit. Physiol. 12: 237-238.