Suppression of cancer phenotypes through a multifunctional actin-binding protein, calponin, that attacks cancer cells and simultaneously protects the host from invasion

Cancer Science

Volumn 96, Issue 11, 2005, Pages 738-746

  Taniguchi, Shun'Ichiro ^a,b  

^a SHINSHU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b KYUSHU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ACTIN BINDING PROTEIN; CALPONIN; CALPONIN H1; UNCLASSIFIED DRUG;

CANCER CELL; CANCER INHIBITION; CANCER INVASION; CANCER PREVENTION; CELL FUNCTION; CELL LINE; CELL TRANSFORMATION; CYTOSKELETON; GENE EXPRESSION REGULATION; GENE TRANSFER; HUMAN; MALIGNANT TRANSFORMATION; MESOTHELIUM CELL; METASTASIS; NONHUMAN; PERITONEUM; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DETERMINATION; PROTEIN FUNCTION; QUALITATIVE ANALYSIS; QUANTITATIVE ANALYSIS; REVIEW; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; SYSTEMATIC REVIEW; TARGET CELL DESTRUCTION; VASCULAR FRAGILITY; VASCULAR SMOOTH MUSCLE; WILD TYPE;

ANIMALS; CALCIUM-BINDING PROTEINS; CELL TRANSFORMATION, NEOPLASTIC; CHEMOPREVENTION; CYTOSKELETAL PROTEINS; DOWN-REGULATION; GENE TRANSFER TECHNIQUES; HUMANS; MICE; MICE, KNOCKOUT; MICROFILAMENT PROTEINS; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; NEOPLASMS, EXPERIMENTAL; NEOVASCULARIZATION, PATHOLOGIC; PHENOTYPE; SIGNAL TRANSDUCTION;

EID: 29644432909     PISSN: 13479032     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1349-7006.2005.00118.x     Document Type: Review

References (72)

1. Taniguchi S, Sagara J, Kakunaga T. Deficient polymerization in vitro of a point-mutated beta-actin expressed in a transformed human fibroblast cell line. J Biochem (Tokyo) 1988; 103: 707-13.
2. Taniguchi S, Kawano T, Kakunaga T, Baba T. Differences in expression of a variant actin between low and high metastatic B16 melanoma. J Biol Chem 1986; 261: 6100-6.
3. Shimokawa-Kuroki R, Sadano H, Taniguchi S. A variant actin (â m) reduces metastasis of mouse B16 melanoma. Int J Cancer 1994; 56: 689-97.
4. Okamoto-Inoue M, Taniguchi S, Sadano H et al. Alteration in expression of smooth muscle alpha-actin associated with transformation of rat 3Y1 cells. J Cell Sci 1990; 96 (Pt 4): 631-7.
5. Okamoto-Inoue M, Kamada S, Kimura G, Taniguchi S. The induction of smooth muscle alpha actin in a transformed rat cell line suppresses malignant properties in vitro and in vivo. Cancer Lett 1999; 142: 173-8.
6. Miyado K, Kimura M, Taniguchi S. Decreased expression of a single tropomyosin isoform, TM5/TM30nm, results in reduction in motility of highly metastatic B16-F10 mouse melanoma cells. Biochem Biophys Res Commun 1996; 225: 427-35.
7. Sadano H, Inoue M, Taniguchi S. Differential expression of vinculin between weakly and highly metastatic B16-melanoma cell lines. Jpn J Cancer Res 1992; 83: 625-30.
8. Sagawa N, Fujita H, Banno Y, Nozawa Y, Katoh H, Kuzumaki N. Gelsolin suppresses tumorigenicity through inhibiting PKC activation in a human lung cancer cell line, PC10. Br J Cancer 2003; 88: 606-12.
9. Horiuchi A, Nikaido T, Taniguchi S, Fujii S. Possible role of calponin h1 as a tumor suppressor in human uterine leiomyosarcoma. J Natl Cancer Inst 1999; 91: 790-6.
10. Takeoka M, Ehara T, Sagara J, Hashimoto S, Taniguchi S. Calponin h1 induced a flattened morphology and suppressed the growth of human fibrosarcoma HT1080 cells. Eur J Cancer 2002; 38: 436-42.
11. Kaneko M, Takeoka M, Oguchi M et al. Calponin h1 suppresses tumor growth of Src-induced transformed 3Y1 cells in association with a decrease in angiogenesis. Jpn J Cancer Res 2002; 93: 935-43.
12. Ramaswamy S, Ross KN, Lander ES, Golub TR. A molecular signature of metastasis in primary solid tumors. Nat Genet 2003; 33: 49-54.
13. Takahashi K, Abe M, Hiwada K, Kokubu T. A novel troponin T-like protein (calponin) in vascular smooth muscle: interaction with tropomyosin paracrystals. J Hypertens 1988; 6: S40-S43.
14. Strasser P, Gimona M, Moessler H, Herzog M, Small JV. Mammalian calponin: identification and expression of genetic variants. FEBS Lett 1993; 330: 13-18.
15. Applegate D, Feng W, Green RS, Taubman MB. Cloning and expression of a novel acidic calponin isoform from rat aortic vascular smooth muscle. J Biol Chem 1994; 269: 10 683-90.
16. Danninger C, Gimona M. Live dynamics of GFP-calponin: isoform-specific modulation of the actin cytoskeleton and autoregulation by C-terminal sequences. J Cell Sci 2000; 113 (Pt 21): 3725-36.
17. Burgstaller G, Kranewitter WJ, Gimona M. The molecular basis for the autoregulation of calponin by isoform-specific C-terminal tail sequences. J Cell Sci 2002; 115 (Pt 10): 2021-9.
18. Wills FL, McCubbin WD, Kay CM. Characterization of the smooth muscle calponin and calmodulin complex. Biochemistry 1993; 32: 2321-8.
19. Shirinsky VP, Biryukov KG, Hettasch JM, Sellers JR. Inhibition of the relative movement of actin and myosin by caldesmon and calponin. J Biol Chem 1992; 267: 15 886-92.
20. Mabuchi K, Li B, Ip W, Tao T. Association of calponin with desmin intermediate filaments. J Biol Chem 1997; 272: 22 662-6.
21. Bogatcheva NV, Gusev NB. Interaction of smooth muscle calponin with phospholipids. FEBS Lett 1995; 371: 123-6.
22. Winder SJ, Walsh MP. Smooth muscle calponin: inhibition of actomyosin MgATPase and regulation by phosphorylation. J Biol Chem 1990; 265: 10 148-55.
23. Stradal T, Kranewitter W, Winder SJ, Gimona M. CH domains revisited. FEBS Lett 1998: 431: 134-7.
24. Mezgueldi M, Mendre C, Calas B, Kassab R, Fattoum A. Characterization of the regulatory domain of gizzard calponin interactions of the 145-163 region with F-actin, calcium-binding proteins, and tropomyosin. J Biol Chem 1995; 270: 8867-76.
25. Mino T, Yuasa U, Nakamura F, Naka M, Tanaka T. Two distinct actin-binding sites of smooth muscle calponin. Eur J Biochem 1998; 251: 262-8.
26. Leinweber BD, Leavis PC, Grabarek Z, Wang CLA, Morgan KG. Extracellular regulated kinase (ERK) interaction with actin and the calponin homology (CH) domain of actin-binding proteins. Biochem J 1999; 344: 117-23.
27. Horowitz A, Clement-Chomienne O, Walsh MP, Tao T, Katsuyama H, Morgan KG. Effects of calponin on force generation by single smooth muscle cells. Am J Physiol 1996; 270: H1858-H1863.
28. Menice CB, Hulvershorn J, Adam LP, Wang CLA, Morgan KG. Calponin and mitogen-activated protein kinase signaling in differentiated vascular smooth muscle. J Biol Chem 1997; 272: 25 157-61.
29. Morgan KG, Gangopadhyay SS. Invited review: Cross-bridge regulation by thin filament-associated proteins. J Appl Physiol 2001; 91: 953-62.
30. Kaneko T, Amano M, Maeda A et al. Identification of calponin as a novel substrate of Rho-kinase. Biochem Biophys Res Commun 2000; 273: 110-16.
31. Takahashi K, Yoshimoto R, Fuchibe K et al. Regulation of shortening velocity by calponin in intact contracting smooth muscles. Biochem Biophys Res Commun 2000; 279: 150-7.
32. Masuki S, Takeoka M, Taniguchi S, Nose H. Enhanced baroreflex sensitivity in free-moving calponin knockout mice. Am J Physiol Heart Circ Physiol 2003; 284: H939-46.
33. Matthew JD, Khromov AS, McDuffie MJ et al. Contractile properties and proteins of smooth muscles of a calponin knockout mouse. J Physiol 2000; 529 (Pt 3): 811-24.
34. Samaha FF, Ip HS, Morrisey EE et al. Developmental pattern of expression and genomic organization of the calponin-h1 gene. A contractile smooth muscle cell marker. J Biol Chem 1996; 271: 395-403.
35. Miano JM, Carlson MJ, Spencer JA, Misra RP. Serum response factor-dependent regulation of the smooth muscle calponin gene. J Biol Chem 2000; 275: 9814-22.
36. Takahashi K, Tazunoki T, Okada T et al. The 5′-flanking region of the human smooth muscle cell calponin gene contains a cis-acting domain for interaction with a methylated DNA-binding transcription repressor. J Biochem (Tokyo) 1996; 120: 18-21.
37. Mano T, Luo Z, Malendowicz SL et al. Reversal of GATA-6 downregulation promotes smooth muscle differentiation and inhibits intimal hyperplasia in balloon-injured rat carotid artery. Circ Res 1999; 84: 647-54.
38. Miralles F, Posern G, Zaromytidou AI, Treisman R. Actin dynamics control SRF activity by regulation of its coactivator MAL. Cell 2003; 113: 329-42.
39. Yamamura H, Yoshikawa H, Takahashi K. Aberrant methylation and silencing of the calponin gene in human sarcoma cells. Anticancer Res 2003; 23: 107-14.
40. Miano JM, Olson EN. Expression of the smooth muscle cell calponin gene marks the early cardiac and smooth muscle cell lineages during mouse embryogenesis. J Biol Chem 1996; 271: 7095-103.
41. Horiuchi A, Nikaido T, Ito K et al. Reduced expression of calponin h1 in leiomyosarcoma of the uterus. Lab Invest 1998; 78: 839-46.
42. Lener T, Burgstaller G, Gimona M. The role of calponin in the gene profile of metastatic cells: inhibition of metastatic cell motility by multiple calponin repeats. FEBS Lett 2004; 556: 221-6.
43. Okamoto-Inoue M, Nakayama J, Hori Y, Taniguchi S. Human malignant melanoma cells release a factor that inhibits the expression of smooth muscle alpha-actin. J Dermatol Sci 2000; 23: 170-7.
44. Kobayashi H, Tsuruchi N, Sugihara K et al. Expression of α-smooth muscle actin in benign or malignant ovarian tumors. Gynecol Oncol 1993; 48: 308-13.
45. Islam AH, Ehara T, Kato H et al. Calponin h1 expression in renal tumor vessels: correlations with multiple pathological factors of renal cell carcinoma. J Urol 2004; 171: 1319-23.
46. Sasaki Y, Yamamura H, Kawakami Y et al. Expression of smooth muscle calponin in tumor vessels of human hepatocellular carcinoma and its possible association with prognosis. Cancer 2002; 94: 1777-86.
47. Hayashi K, Saga H, Chimori Y, Kimura K, Yamanaka Y, Sobue K. Differentiated phenotype of smooth muscle cells depends on signaling pathways through insulin-like growth factors and phosphatidylinositol 3-kinase. J Biol Chem 1998; 273: 28 860-7.
48. Hansson GK, Hellstrand M, Rymo L, Rubbia L, Gabbiani G. Interferon gamma inhibits both proliferation and expression of differentiation-specific alpha-smooth muscle actin in arterial smooth muscle cells. J Exp Med 1989; 170: 1595-608.
49. Koganehira Y, Takeoka M, Ehara T et al. Reduced expression of actin-binding proteins, h-caldesmon and calponin h1, in the vascular smooth muscle inside melanoma lesions: an adverse prognostic factor for malignant melanoma. Br J Dermatol 2003; 148: 971-80.
50. Taniguchi S, Takeoka M, Ehara T et al. Structural fragility of blood vessels and peritoneum in calponin h1-deficient mice, resulting in an increase in hematogenous metastasis and peritoneal dissemination of malignant tumor cells. Cancer Res 2001; 61: 7627-34.
51. Sakihara C, Nishimura J, Kobayashi S, Takahashi S, Kanaide H. Expression of calponin mRNA in porcine aortic endothelial cells. Biochem Biophys Res Commun 1996; 222: 195-200.
52. Hashimoto S, Takeoka M, Taniguchi S. Suppression of peritoneal dissemination through protecting mesothelial cells from retraction by cancer cells. Int J Cancer 2003; 107: 557-63.
53. Horiuchi A, Nikaido T, Ya-Li Z, Ito K, Orii A, Fujii S. Heparin inhibits proliferation of myometrial and leiomyomal smooth muscle cells through the induction of alpha-smooth muscle actin, calponin h1 and p27. Mol Hum Reprod 1999; 5: 139-45.
54. Masumoto J, Taniguchi S, Ayukawa K et al. ASC, a novel 22-kDa protein, aggregates during apoptosis of human promyelocytic leukemia HL-60 cells. J Biol Chem 1999; 274: 33 835-8.
55. Ancient missense mutations in a new member of the RoRet gene family are likely to cause familial Mediterranean fever. The International FMF Consortium. Cell 1997; 90: 797-807.
56. Masumoto J, Taniguchi S, Sagara J. Pyrin N-terminal homology domain- and caspase recruitment domain-dependent oligomerization of ASC. Biochem Biophys Res Commun 2001; 280: 652-5.
57. Moriya M, Taniguchi S, Wu P, Liepinsh E, Otting G, Sagara J. Role of charged and hydrophobic residues in the oligomerization of the PYRIN domain of ASC. Biochemistry 2005; 44: 575-83.
58. Masumoto J, Taniguchi S, Nakayama J et al. Expression of apoptosis-associated speck-like protein containing a caspase recruitment domain, a pyrin N-terminal homology domain-containing protein, in normal human tissues. J Histochem Cytochem 2001; 49: 1269-75.
59. Shiohara M, Taniguchi S, Masumoto J et al. ASC, which is composed of a PYD and a CARD, is up-regulated by inflammation and apoptosis in human neutrophils. Biochem Biophys Res Commun 2002; 293: 1314-8.
60. Bertin J, DiStefano PS. The PYRIN domain: a novel motif found in apoptosis and inflammation proteins. Cell Death Differ 2000: 7: 1273-4.
61. Feldmann J, Prieur AM, Quartier P et al. Chronic infantile neurological cutaneous and articular syndrome is caused by mutations in CIAS1, a gene highly expressed in polymorphonuclear cells and chondrocytes. Am J Hum Genet 2002; 71: 198-203.
62. Stehlik C, Lee SH, Dorfleutner A, Stassinopoulos A, Sagara J, Reed JC. Apoptosis-associated speck-like protein containing a caspase recruitment domain is a regulator of procaspase-1 activation. J Immunol 2003; 171: 6154-63.
63. Martinon F, Burns K, Tschopp J. The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-beta. Mol Cell 2002; 10: 417-26.
64. Martinon F, Tschopp J. Inflammatory caspases: linking an intracellular innate immune system to autoinflammatory diseases. Cell 2004: 117: 561-74.
65. Stehlik C, Reed JC. The PYRIN connection: novel players in innate immunity and inflammation. J Exp Med 2004; 200: 551-8.
66. Yamamoto M, Yaginuma K, Tsutsui H et al. ASC is essential for LPS-induced activation of procaspase-1 independently of TLR-associated signal adaptor molecules. Genes Cells 2004; 9: 1055-67.
67. Mariathasan S, Newton K, Monack DM et al. Differential activation of the inflammasome by caspase-1 adaptors ASC and Ipaf. Nature 2004; 430: 213-8.
68. McConnell BB, Vertino PM. TMS1/ASC: the cancer connection. Apoptosis 2004: 9: 5-18.
69. Conway KE, McConnell BB, Bowring CE, Donald CD, Warren ST, Vertino PM. TMS1, a novel proapoptotic caspase recruitment domain protein, is a target of methylation-induced gene silencing in human breast cancers. Cancer Res 2000; 60: 6236-42.
70. Yokoyama T, Sagara J, Guan X et al. Methylation of ASC/TMS1, a proapoptotic gene responsible for activating procaspase-1, in human colorectal cancer. Cancer Lett 2003; 202: 101-8.
71. Guan X, Sagara J, Yokoyama T et al. ASC/TMS1, a caspase-1 activating adaptor, is downregulated by aberrant methylation in human melanoma. Int J Cancer 2003; 107: 202-8.
72. Ohtsuka T, Ryu H, Minamishima YA et al. ASC is a Bax adaptor and regulates the p53-Bax mitochondrial apoptosis pathway. Nat Cell Biol 2004; 6: 121-8.