Sains Malaysiana 49(6)(2020): 1351-1358

http://dx.doi.org/10.17576/jsm-2020-4906-13

 

Role of Novel Therapeutic Agents in Modulating Invadopodia Formation in Metastatic Breast Cancer

(Peranan Agen Terapi Baru dalam Memodulasikan Pembentukan Invadopodia dalam Kanser Payudara Metastatik)

 

SITI NOR AINI HARUN1, NURUL AKMARYANTI ABDULLAH1, NORAINA MUHAMAD ZAKUAN1, HAFIZAH ABDUL HAMID1, MUHAMMAD ZULFADLI MEHAT2 & NUR FARIESHA MD HASHIM1*

 

1Department of Biomedical Sciences, Faculty of Medicine and Health Sciences, Universiti Putra Malaysia, 43400 UPM Serdang, Selangor Darul Ehsan, Malaysia

 

2Department of Human Anatomy, Faculty of Medicine and Health Sciences, Universiti Putra Malaysia, 43400 UPM Serdang, Selangor Darul Ehsan, Malaysia

 

Received: 12 July 2019/Accepted: 11 February 2020

 

ABSTRACT

The ability to colonize distant organs which is lethal has made metastatic breast cancer become the top ten causes of mortality worldwide. Specialized actin-rich protrusions termed invadopodia were thought to be formed by highly invasive cells to degrade the extracellular matrix to drive cancer invasion and metastasis. Identification of compound(s) to hinder the formation ofinvadopodia is important to resist the metastasis of breast cancer as well as to yield anti-metastasis targeted therapy. The current review aims to provide new insights on cancer invasion and candidate compound(s) capable to disrupt invadopodia formation and invadopodia-related proteins.

 

Keywords: Cancer invasion; invadopodia; metastatic breast cancer

 

ABSTRAK

Keupayaan untuk merebak ke organ lain telah menjadikan kanser payudara metastatik antara puluhan penyebab kematian di seluruh dunia. Protusi khusus diperkaya-aktin ataupun invadopodia dikatakan terbentuk daripada sel-sel yang invasif sehingga mendegradasi matriks ekstrasel yang seterusnya mendorong kepada serangan kanser dan metastasis. Pengenalpastian kompaun untuk menghalang pembentukan invadopodia adalah penting untuk menentang kanser payudara metastatik serta mencari terapi sasaran anti-metastatik. Ulasan ini bertujuan untuk memberikan pandangan baru mengenai serangan kanser dan kompaun yang berkemungkinan menghalang pembentukan invadopodia dan protein berkaitan dengan invadopodia.

 

Kata kunci: Invadopodia; kanser payudara metastatik; serangan kanser

 

REFERENCES

Anand, P., Kunnumakkara, A.B., Newman, R.A. & Aggarwal, B.B. 2007. Bioavailability of curcumin: Problems and promises. Molecular Pharmaceutics 4(6): 807-818.

Anders, C. & Carey, L.A. 2008. Understanding and treating triple-negative breast cancer. Oncology (Williston Park) 22(11): 1233-1243.

Artym, V.V., Zhang, Y., Seillier-Moiseiwitsch, F., Yamada, K.M. & Mueller, S.C. 2006. Dynamic interactions of cortactin and membrane type 1 matrix metalloproteinase at invadopodia: Defining the stages of invadopodia formation and function. Cancer Research 66(6): 3034-3043.

Azizah, A.M., Ibrahim, N.S. & Abdullah, N.H. 2015. Malaysian National Cancer Registry Report 2007-2011. Putrajaya: Ministry of Health, Malaysia.

Balzer, E.M., Whipple, R.A., Thompson, K., Boggs, A.E., Slovic, J., Cho, E.H., Matrone, M.A., Yoneda, T., Mueller, S.C. & Martin, S.S. 2010. c-Src differentially regulates the functions of microtentacles and invadopodia. Oncogene 29(48): 6402-6408.

Bergamo, A., Masi, A., Peacock, A.F.A., Habtemariam, A., Sadler, P.J. & Sava, G. 2010. In vivo tumour and metastasis reduction and in vitro effects on invasion assays of the ruthenium RM175 and osmium AFAP51 organometallics in the mammary cancer model. Journal of Inorganic Biochemistry 104(1): 79-86.

Bravo-Cordero, J.J., Hodgson, L. & Condeelis, J. 2012. Directed cell invasion and migration during metastasis. Current Opinion in Cell Biology 24(2): 277-283.

Buccione, R., Orth, J.D. & McNiven, M.A. 2004. Foot and mouth: Podosomes, invadopodia and circular dorsal ruffles. Nature Reviews Molecular Cell Biology 5(8): 647-657.

Chen, Q., Zheng, Y., Jiao, D., Chen, F., Hu, H., Wu, Y., Song, J., Yan, J., Wu, L. & Lv, G. 2014. Curcumin inhibits lung cancer cell migration and invasion through Rac1-dependent signaling pathway. The Journal of Nutritional Biochemistry 25(2): 177-185.

Chen, Q.Y., Jiao, D.M., Yao, Q.H., Yan, J., Song, J., Chen, F.Y., Lu, G.H. & Zhou, J.Y. 2012. Expression analysis of Cdc42 in lung cancer and modulation of its expression by curcumin in lung cancer cell lines. International Journal of Oncology 40(5): 1561-1568.

Chen, W.T. 1989. Proteolytic activity of specialized surface protrusions formed at rosette contact sites of transformed cells. Journal of Experimental Zoology 251(2): 167-185.

Cheung, K.J. & Ewald, A.J. 2016. A collective route to metastasis: Seeding by tumor cell clusters. Science 352(6282): 167-169.

Chevalier, C., Collin, G., Descamps, S., Touaitahuata, H., Simon, V., Reymond, N., Fernandez, L., Milhiet, P.E., Georget, V., Urbach, S., Lasorsa, L., Orsetti, B., Boissière-Michot, F., Lopez-Crapez, E., Theillet, C., Roche, S. & Benistant, C. 2016. TOM1L1 drives membrane delivery of MT1-MMP to promote ERBB2-induced breast cancer cell invasion. Nature Communications 7(1): 1-16.

Chhabra, E.S. & Higgs, H.N. 2007. The many faces of actin: matching assembly factors with cellular structures. Nature Cell Biology 9(10): 1110-1121.

Chiu, T-L. & Su, C-C. 2009. Curcumin inhibits proliferation and migration by increasing the Bax to Bcl-2 ratio and decreasing NF-kBp65 expression in breast cancer MDA-MB-231 cells. International Journal of Molecular Medicine 23(4): 469-475.

Clark, E.S., Whigham, A.S., Yarbrough, W.G. & Weaver, A.M. 2007. Cortactin is an essential regulator of matrix metalloproteinase secretion and extracellular matrix degradation in   invadopodia. Cancer Research 67(9): 4227-4235.

David-Pfeuty, T. & Singer, S.J. 1980. Altered distributions of the cytoskeletal proteins vinculin and alpha-actinin in cultured fibroblasts transformed by Rous sarcoma virus. Proceedings of the National Academy of Sciences of the United States of America 77(11): 6687-6691.

Dent, R., Trudeau, M., Pritchard, K.I., Hanna, W.M., Kahn, H.K., Sawka, C.A., Lickley, L.A., Rawlinson, E., Sun, P. & Narod, S.A. 2007. Triple-negative breast cancer: Clinical features and patterns of recurrence. Clinical Cancer Research 13(15): 4429-4434.

Di, G.H., Li, H.C., Shen, Z.Z. & Shao, Z.M. 2003. Analysis of anti-proliferation of curcumin on human breast cancer cells and its mechanism. Zhonghua Yi Xue Za Zhi 83(20): 1764-1768.

Di Martino, J., Paysan, L., Gest, C., Lagrée, V., Juin, A., Saltel, F. & Moreau, V 2014. Cdc42 and Tks5: A minimal and universal molecular signature for functional invadosomes. Cell Adhesion & Migration 8(3): 280-292.

Díaz, B., Yuen, A., Iizuka, S., Higashiyama, S. & Courtneidge, S.A. 2013. Notch increases the shedding of HB-EGF by ADAM12 to potentiate invadopodia formation in hypoxia. Journal of Cell Biology 201(2): 279-292.

Doyle, A.D., Petrie, R.J., Kutys, M.L. & Yamada, K.M. 2013. Dimensions in cell migration. Current Opinion in Cell Biology 25(5): 642-649.

Egeblad, M. & Werb, Z. 2002. New functions for the matrix metalloproteinases in cancer progression. Nature Reviews Cancer 2(3): 161-174.

Fu, H., Wu, R., Li, Y., Zhang, L., Tang, X., Tu, J., Zhou, W., Wang, J. & Shou, Q. 2016. Safflower yellow prevents pulmonary metastasis of breast cancer by inhibiting tumor cell invadopodia. The American Journal of Chinese Medicine 44(7): 1491-1506.

Gligorijevic, B., Wyckoff, J., Yamaguchi, H., Wang, Y., Roussos, E.T. & Condeelis, J. 2012. N-WASP-mediated invadopodium formation is involved in intravasation and lung metastasis of mammary tumors. Journal of Cell Science 125(3): 724-734.

Gujam, F.J.A., Going, J.J., Mohammed, Z.M.A., Orange, C., Edwards, J. & McMillan, D.C. 2014. Immunohistochemical detection improves the prognostic value of lymphatic and blood vessel invasion in primary ductal breast cancer. BMC cancer 14(1): 676.

Gupta, S.C., Patchva, S., Koh, W. & Aggarwal, B.B. 2012. Discovery of curcumin, a component of golden spice, and its miraculous biological activities. Clinical and Experimental Pharmacology and Physiology 39(3): 283-299.

Hall, A. 1998. Rho GTPases and the actin cytoskeleton. Science 279(5350): 509-514.

Hanahan, D. & Weinberg, R.A. 2011. Hallmarks of cancer: The next generation. Cell 144(5): 646-674.

Harun, S.N.A., Israf, D.A., Tham, C.L., Lam, K.W., Cheema, M.S. & Hashim, N.F.M. 2018. The molecular targets and anti-invasive effects of 2,6-bis-(4-hydroxyl-3methoxybenzylidine) cyclohexanone or BHMC in MDA-MB-231 human breast cancer cells. Molecules 23(4): 865.

Hassan, Z.K. & Daghestani, M.H. 2012. Curcumin effect on MMPs and TIMPs genes in a breast cancer cell line. Asian Pacific Journal of Cancer Prevention 13(7): 3259-3264.

Hoshino, D., Branch, K.M. & Weaver, A.M. 2013. Signaling inputs to invadopodia and podosomes. Journal of Cell Science 126(14): 2979-2989.

Ichikawa, K. 2015. Synergistic effect of blocking cancer cell invasion revealed by computer simulations. Mathematical Biosciences and Engineering 12(6): 1189-1202.

Jiang, P., Enomoto, A. & Takahashi, M. 2009. Cell biology of the movement of breast cancer cells: Intracellular signalling and the actin cytoskeleton. Cancer Letter 284(2): 122-130.

Koo, H.J., Shin, S., Choi, J.Y., Lee, K.H., Kim, B.T. & Choe, Y.S. 2015. Introduction of methyl groups at C2 and C6 positions enhances the antiangiogenesis activity of curcumin. Scientific Reports 5: 14205.

Krausz, A.E., Adler, B.L., Cabral, V., Navati, M., Doerner, J., Charafeddine, R.A., Chandra, D., Liang, H., Gunther, L., Clendaniel, A., Harper, S., Friedman, J.M., Nosanchuk, J.D. & Friedman, A.J. 2015. Curcumin-encapsulated nanoparticles as innovative antimicrobial and wound healing agent. Nanomedicine: Nanotechnology, Biology, and Medicine 11(1): 195-206.

Kuo, J.C., Han, X., Hsiao, C.T., Yates, J.R. & Waterman, C.M. 2011. Analysis of the myosin-II-responsive focal adhesion proteome reveals a role for β-Pix in negative regulation of focal adhesion maturation. Nature Cell Biology 13(4): 383-395.

Langley, R.R. & Fidler, I.J. 2011. The seed and soil hypothesis revisited - The role of tumorstroma interactions in metastasis to different organs. International Journal of Cancer 128(11): 2527-2535.

Lee, W.H., Loo, C.Y., Young, P.M., Rohanizadeh, R. & Traini, D. 2016. Curcumin nanoparticles attenuate production of pro-inflammatory markers in lipopolysaccharide-induced macrophages. Pharmaceutical Research 33(2): 315-327.

Linder, S. & Aepfelbacher, M. 2003. Podosomes: Adhesion hot-spots of invasive cells. Trends in Cell Biology 13(7): 376-385.

Liotta, L.A., Steeg, P.S. & Stetler-Stevenson, W.G. 1991. Cancer metastasis and angiogenesis: An imbalance of positive and negative regulation. Cell 64(2): 327-336.

Lohmer, L.L., Kelley, L.C., Hagedorn, E.J. & Sherwood, D.R. 2014. Invadopodia and basement membrane invasion in vivo. Cell Adhesion & Migration 8(3): 246-255.

Mader, C.C., Oser, M., Magalhaes, M.A.O., Bravo-Cordero, J.J., Condeelis, J., Koleske, A.J. & Gil-Henn, H. 2011. An EGFR-Src-Arg-Cortactin pathway mediates functional maturation of invadopodia and breast cancer cell invasion. Cancer Research 71(5): 1730-1741.

Massagué, J., Batlle, E. & Gomis, R.R. 2017. Understanding the molecular mechanisms driving metastasis. Molecular Oncology 11(1): 3-4.

Md Hashim, N.F., Nicholas, N.S., Dart, A.E., Kiriakidis, S., Paleolog, E. & Wells, C.M. 2013. Hypoxia-induced invadopodia formation: A role for -PIX. Open Biology 3(6): 120159-120159.

Mendonsa, A.M., Na, T.Y. & Gumbiner, B.M. 2018. E-cadherin in contact inhibition and cancer. Oncogene 37(35): 4769-4780.

Ming-Tatt, L., Khalivulla, S.I., Akhtar, M.N., Lajis, N., Perimal, E.K., Akira, A., Ali, D.I. & Sulaiman, M.R. 2013. Anti-hyperalgesic effect of a benzilidine-cyclohexanone analogue on a mouse model of chronic constriction injury-induced neuropathic pain: Participation of the κ-Opioid receptor and KATP. Pharmacology Biochemistry and Behavior 114-115: 58-63.

Miyazawa, Y., Uekita, T., Ito, Y., Seiki, M., Yamaguchi, H. & Sakai, R. 2013. CDCP1 regulates the function of MT1-MMP and invadopodia-mediated invasion of cancer cells. Molecular Cancer Research 11(6): 628-637.

Murphy, D.A. & Courtneidge, S.A. 2011. The ‘ins’ and ‘outs’ of podosomes and invadopodia: Characteristics, formation and function. Nature Reviews Molecular Cell Biology 12(7): 413-426.

Neil, J.R. & Schiemann, W.P. 2008. Altered TAB1: IKK interaction promotes TGF-β-mediated NF-κB activation during breast cancer progression. Cancer research 68(5): 1462-1470.

Orsetti, B., Nugoli, M., Cervera, N., Lasorsa, L., Chuchana, P., Ursule, L., Nguyen, C., Redon, R., Du Manoir, S., Rodriguez, C. & Theillet, C. 2004. Genomic and expression profiling of chromosome 17 in breast cancer reveals complex patterns of alterations and novel candidate genes. Cancer Research 64(18): 6453-6460.

Paget, S. 1889. The distribution of secondary growths in cancer of the breast. The Lancet 133(3421): 571-573.

Pollard, T.D. & Borisy, G.G. 2003. Cellular motility driven by assembly and disassembly of actin filaments. Cell 112(4): 453-465.

Poste, G. & Fidler, I.J. 1980. The pathogenesis of cancer metastasis. Nature 283(5743): 139-146.

Razak, N.A., Akhtar, M.N., Abu, N., Ho, W.Y., Tan, S.W., Zareen, S., Taj-ud-din, S.N. bin, Long, K., Alitheen, N.B. & Yeap, S.K. 2017. The in vivo anti-tumor effect of curcumin derivative (2E{,}6E)-2{,}6-bis(4-hydroxy-3-methoxybenzylidene)cyclohexanone (BHMC) on 4T1 breast cancer cells. RSC Advance 7(57): 36185-36192.

Revach, O.Y., Winograd-Katz, S.E., Samuels, Y. & Geiger, B. 2016. The involvement of mutant Rac1 in the formation of invadopodia in cultured melanoma cells. Experimental Cell Research 343(1): 82-88.

Ridley, A.J. 2015. Rho GTPase signalling in cell migration. Current Opinion in Cell Biology 36: 103-112.

Riggi, N., Aguet, M. & Stamenkovic, I. 2018. Cancer metastasis: A reappraisal of its underlying mechanisms and their relevance to treatment. Annual Review of Pathology: Mechanisms of Disease 13: 117-140.

Sahai, E. 2005. Mechanisms of cancer cell invasion. Current Opinion in Genetics & Development 15(1): 87-96.

Schnoor, M., Stradal, T.E. & Rottner, K. 2017. Cortactin: Cell functions of a multifaceted actin-binding protein. Trends in Cell Biology 28(2): 79-98.

Scolaro, C., Bergamo, A., Brescacin, L., Delfino, R., Cocchietto, M., Laurenczy, G., Geldbach, T.J., Sava, G. & Dyson, P.J. 2005. In vitro and in vivo evaluation of ruthenium (II)- arene PTA complexes. Journal of Medicinal Chemistry 48(12): 4161-4171.

Scully, O.J., Bay, B.H., Yip, G. & Yu, Y. 2012. Breast cancer metastasis. Cancer Genomics-Proteomics 9(5): 311-320.

Shao, Z.M., Shen, Z.Z., Liu, C.H., Sartippour, M.R., Go, V.L., Heber, D. & Nguyen, M. 2002. Curcumin exerts multiple suppressive effects on human breast carcinoma cells. International Journal of Cancer 98(2): 234-240.

Shen, H.L., Liu, Q.J., Yang, P.Q. & Tian, Y. 2015. Protein interactions of cortactin in relation to invadopodia formation in metastatic renal clear cell carcinoma. Tumor Biology 36(5): 3417-3422.

Smid, M., Wang, Y., Klijn, J.G.M., Sieuwerts, A.M., Zhang, Y., Atkins, D., Martens, J.W.M. & Foekens, J.A. 2006. Genes associated with breast cancer metastatic to bone. Journal of Clinical Oncology 24(15): 2261-2267.

Steeg, P.S. 2016. Targeting metastasis. Nature Reviews Cancer 16(4): 201-218.

Sun, K., Duan, X., Cai, H., Liu, X., Yang, Y., Li, M., Zhang, X. & Wang, J. 2016. Curcumin inhibits LPA-induced invasion by attenuating RhoA/ROCK/MMPs pathway in MCF7 breast cancer cells. Clinical and Experimental Medicine 16(1): 37-47.

Tang, D., Tao, D., Fang, Y., Deng, C., Xu, Q. & Zhou, J. 2017. TNF-alpha promotes invasion and metastasis via NF-kappa B pathway in oral squamous cell carcinoma. Medical Science Monitor Basic Research 23: 141-149.

Tarone, G., Cirillo, D., Giancotti, F.G., Comoglio, P.M. & Marchisio, P.C. 1985. Rous sarcoma virus-transformed fibroblasts adhere primarily at discrete protrusions of the ventral membrane called podosomes. Experimental Cell Research 159(1): 141-157.

Tham, C.L., Lam, K.W., Rajajendram, R., Cheah, Y.K., Sulaiman, M.R., Lajis, N.H., Kim, M.K. & Israf, D.A. 2011. The effects of a synthetic curcuminoid analogue, 2,6-bis-(4-hydroxyl-3-methoxybenzylidine)cyclohexanone on proinflammatory signaling pathways and CLP-induced lethal sepsis in mice. European Journal of Pharmacology 652(1-3): 136-144.

Tham, C.L., Liew, C.Y., Lam, K.W., Mohamad, A.S., Kim, M.K., Cheah, Y.K., Zakaria, Z.A., Sulaiman, M.R., Lajis, N.H. & Israf, D.A. 2010. A synthetic curcuminoid derivative inhibits nitric oxide and proinflammatory cytokine synthesis. European Journal of Pharmacology 628(1-3): 247-254.

Tolde, O., Rösel, D., Veselý, P., Folk, P. & Brábek, J. 2010. The structure of invadopodia in a complex 3D environment. European Journal of Cell Biology 89(9): 674-680.

Wang, S., Li, E., Gao, Y., Wang, Y., Guo, Z., He, J., Zhang, J., Gao, Z. & Wang, Q. 2013. Study on invadopodia formation for lung carcinoma invasion with a microfluidic 3D culture device. PLoS ONE 8(2): e56448.

Wang, T., Liu, N.S., Seet, L.F. & Hong, W. 2010. The emerging role of VHS domain containing Tom1, Tom1L1 and Tom1L2 in membrane trafficking. Traffic 11(9): 1119-1128.

Wang, Z., Liang, X., Cai, M. & Du, G. 2016. Analysis of invadopodia formation in breast cancer cells. Methods in Molecular Biology 1406: 203-210.

Ward, J.D., Ha, J.H., Jayaraman, M. & Dhanasekaran, D.N. 2015. LPA-mediated migration of ovarian cancer cells involves translocalization of Gαi2to invadopodia and association with Src and β-pix. Cancer Letters 356(2): 382-391.

Weigelt, B., Peterse, J.L. & Van’t Veer, L.J. 2005. Breast cancer metastasis: Markers and models. Nature Reviews Cancer 5(8): 591-602.

Wu, Q., He, J., Mei, W., Zhang, Z., Wu, X. & Sun, F. 2014. Arene ruthenium (II) complex, a potent inhibitor against proliferation, migration and invasion of breast cancer cells, reduces stress fibers, focal adhesions and invadopodia. Metallomics 6(12): 2204-2212.

Zambonin, A., Teti, A., Carano, A. & Marchisio, P.C. 1988. The distribution of podosomes in osteoclasts cultured on bone laminae: Effect of retinol. Journal of Bone and Mineral Research 3(5): 517-523.

 

*Corresponding author; email: nurfariesha@upm.edu.my

 

 

 

 

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