The extracellular matrix enriched with membrane metalloendopeptidase and insulin-degrading enzyme suppresses the deposition of amyloid-beta peptide in Alzheimer's disease cell models
Shumang Zhang
CAS Key Laboratory of Nano-Bio Interface, Suzhou Institute of Nano-Tech and Nano-Bionics, Chinese Academy of Sciences, Jiangsu, China
School of Life Sciences, Shanghai University, Shanghai, China
Search for more papers by this authorTongqian Xiao
CAS Key Laboratory of Nano-Bio Interface, Suzhou Institute of Nano-Tech and Nano-Bionics, Chinese Academy of Sciences, Jiangsu, China
University of Chinese Academy of Sciences, Beijing, China
Search for more papers by this authorYanzhen Yu
CAS Key Laboratory of Nano-Bio Interface, Suzhou Institute of Nano-Tech and Nano-Bionics, Chinese Academy of Sciences, Jiangsu, China
School of Nano-Tech and Nano-Bionics, University of Science and Technology of China, Hefei, China
Search for more papers by this authorYong Qiao
CAS Key Laboratory of Nano-Bio Interface, Suzhou Institute of Nano-Tech and Nano-Bionics, Chinese Academy of Sciences, Jiangsu, China
Search for more papers by this authorZhongjuan Xu
CAS Key Laboratory of Nano-Bio Interface, Suzhou Institute of Nano-Tech and Nano-Bionics, Chinese Academy of Sciences, Jiangsu, China
School of Nano-Tech and Nano-Bionics, University of Science and Technology of China, Hefei, China
Search for more papers by this authorJunsa Geng
CAS Key Laboratory of Nano-Bio Interface, Suzhou Institute of Nano-Tech and Nano-Bionics, Chinese Academy of Sciences, Jiangsu, China
School of Nano-Tech and Nano-Bionics, University of Science and Technology of China, Hefei, China
Search for more papers by this authorYu Liang
CAS Key Laboratory of Nano-Bio Interface, Suzhou Institute of Nano-Tech and Nano-Bionics, Chinese Academy of Sciences, Jiangsu, China
School of Life Sciences, Shanghai University, Shanghai, China
Search for more papers by this authorQun Dong
Department of Pathology, Taikang Xianlin Drum Tower Hospital, Nanjing, China
Search for more papers by this authorBin Wang
Center for Clinic Stem Cell Research, The Affiliated Drum Tower Hospital of Nanjing University Medical School, Nanjing, China
Search for more papers by this authorJiali Wei
School of Life Sciences, Shanghai University, Shanghai, China
Search for more papers by this authorCorresponding Author
Guangli Suo
CAS Key Laboratory of Nano-Bio Interface, Suzhou Institute of Nano-Tech and Nano-Bionics, Chinese Academy of Sciences, Jiangsu, China
Correspondence
Guangli Suo, Suzhou Institute of Nano-Tech and Nano-Bionics, Chinese Academy of Sciences, 398 Ruoshui Road, Suzhou Industrial Park, Suzhou, Jiangsu Province 215123, China.
Email: [email protected]
Search for more papers by this authorShumang Zhang
CAS Key Laboratory of Nano-Bio Interface, Suzhou Institute of Nano-Tech and Nano-Bionics, Chinese Academy of Sciences, Jiangsu, China
School of Life Sciences, Shanghai University, Shanghai, China
Search for more papers by this authorTongqian Xiao
CAS Key Laboratory of Nano-Bio Interface, Suzhou Institute of Nano-Tech and Nano-Bionics, Chinese Academy of Sciences, Jiangsu, China
University of Chinese Academy of Sciences, Beijing, China
Search for more papers by this authorYanzhen Yu
CAS Key Laboratory of Nano-Bio Interface, Suzhou Institute of Nano-Tech and Nano-Bionics, Chinese Academy of Sciences, Jiangsu, China
School of Nano-Tech and Nano-Bionics, University of Science and Technology of China, Hefei, China
Search for more papers by this authorYong Qiao
CAS Key Laboratory of Nano-Bio Interface, Suzhou Institute of Nano-Tech and Nano-Bionics, Chinese Academy of Sciences, Jiangsu, China
Search for more papers by this authorZhongjuan Xu
CAS Key Laboratory of Nano-Bio Interface, Suzhou Institute of Nano-Tech and Nano-Bionics, Chinese Academy of Sciences, Jiangsu, China
School of Nano-Tech and Nano-Bionics, University of Science and Technology of China, Hefei, China
Search for more papers by this authorJunsa Geng
CAS Key Laboratory of Nano-Bio Interface, Suzhou Institute of Nano-Tech and Nano-Bionics, Chinese Academy of Sciences, Jiangsu, China
School of Nano-Tech and Nano-Bionics, University of Science and Technology of China, Hefei, China
Search for more papers by this authorYu Liang
CAS Key Laboratory of Nano-Bio Interface, Suzhou Institute of Nano-Tech and Nano-Bionics, Chinese Academy of Sciences, Jiangsu, China
School of Life Sciences, Shanghai University, Shanghai, China
Search for more papers by this authorQun Dong
Department of Pathology, Taikang Xianlin Drum Tower Hospital, Nanjing, China
Search for more papers by this authorBin Wang
Center for Clinic Stem Cell Research, The Affiliated Drum Tower Hospital of Nanjing University Medical School, Nanjing, China
Search for more papers by this authorJiali Wei
School of Life Sciences, Shanghai University, Shanghai, China
Search for more papers by this authorCorresponding Author
Guangli Suo
CAS Key Laboratory of Nano-Bio Interface, Suzhou Institute of Nano-Tech and Nano-Bionics, Chinese Academy of Sciences, Jiangsu, China
Correspondence
Guangli Suo, Suzhou Institute of Nano-Tech and Nano-Bionics, Chinese Academy of Sciences, 398 Ruoshui Road, Suzhou Industrial Park, Suzhou, Jiangsu Province 215123, China.
Email: [email protected]
Search for more papers by this authorAbstract
Amyloid plaque is a typical feature of Alzheimer's disease (AD) and is one of the targets for AD therapy. Membrane metalloendopeptidase (MME) and insulin-degrading enzyme (IDE) are two types of proteases that could cleave beta-amyloid (Aβ) peptides generated by neuron cells of AD patients. Extracellular matrix (ECM) plays a crucial role in regulating tissue-specific functions and is an ideal biomaterial for tissue repair. In this study, we extracted the liquid ECM enriched with collagen-binding-domain-fused IDE or MME from human foreskin fibroblast cells. We found that these ECM biomaterials reduced the aggregation of Aβ peptides, prevented the formation of amyloid plaques, and also suppressed phosphorylation of Tau protein in AD cell models. Overall, our research provides a novel ECM biomaterial that can be potentially used for AD therapy.
CONFLICT OF INTEREST
The authors have declared that there is no conflict of interest.
Supporting Information
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| term2906_sup-0001-st1.docxWord 2007 document , 16.3 KB |
Table S1. The primers for PCR. |
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REFERENCES
- Benders, K. E., van Weeren, P. R., Badylak, S. F., Saris, D. B., Dhert, W. J., & Malda, J. (2013). Extracellular matrix scaffolds for cartilage and bone regeneration. Trends in Biotechnology, 31, 169–176. https://doi.org/10.1016/j.tibtech.2012.12.004
- Canter, R. G., Penney, J., & Tsai, L. H. (2016). The road to restoring neural circuits for the treatment of Alzheimer's disease. Nature, 539, 187–196. https://doi.org/10.1038/nature20412
- Chen, P. T., Liao, T. Y., Hu, C. J., Wu, S. T., Wang, S. S., & Chen, R. P. (2010). A highly sensitive peptide substrate for detecting two ASS-degrading enzymes: Neprilysin and insulin-degrading enzyme. Journal of Neuroscience Methods, 190, 57–62. https://doi.org/10.1016/j.jneumeth.2010.04.024
- Choi, S. H., Kim, Y. H., Hebisch, M., Sliwinski, C., Lee, S., D'Avanzo, C., … Kim, D. Y. (2014). A three-dimensional human neural cell culture model of Alzheimer's disease. Nature, 515, 274–278. https://doi.org/10.1038/nature13800
- de Souza, S. J., & Brentani, R. (1992). Collagen binding site in collagenase can be determined using the concept of sense-antisense peptide interactions. The Journal of Biological Chemistry, 267, 13763–13767.
- Decaris, M. L., Mojadedi, A., Bhat, A., & Leach, J. K. (2012). Transferable cell-secreted extracellular matrices enhance osteogenic differentiation. Acta Biomaterialia, 8, 744–752. https://doi.org/10.1016/j.actbio.2011.10.035
- Farris, W., Mansourian, S., Chang, Y., Lindsley, L., Eckman, E. A., Frosch, M. P., … Guenette, S. (2003). Insulin-degrading enzyme regulates the levels of insulin, amyloid beta-protein, and the beta-amyloid precursor protein intracellular domain in vivo. Proceedings of the National Academy of Sciences of the United States of America, 100, 4162–4167. https://doi.org/10.1073/pnas.0230450100
- Fitzjohn, S. M., Morton, R. A., Kuenzi, F., Rosahl, T. W., Shearman, M., Lewis, H., … Seabrook, G. R. (2001). Age-related impairment of synaptic transmission but normal long-term potentiation in transgenic mice that overexpress the human APP695swe mutant form of amyloid precursor protein. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 21, 4691–4698. https://doi.org/10.1523/JNEUROSCI.21-13-04691.2001
- Gotz, J., Chen, F., van Dorpe, J., & Nitsch, R. M. (2001). Formation of neurofibrillary tangles in P301L tau transgenic mice induced by Abeta 42 fibrils. Science, 293, 1491–1495. https://doi.org/10.1126/science.1062097
- Grimm, M. O., Mett, J., Stahlmann, C. P., Haupenthal, V. J., Zimmer, V. C., & Hartmann, T. (2013). Neprilysin and Abeta clearance: Impact of the APP intracellular domain in nep regulation and implications in Alzheimer's disease. Frontiers in Aging Neuroscience, 5, 98. https://doi.org/10.3389/fnagi.2013.00098
- Guan, H., Chow, K. M., Shah, R., Rhodes, C. J., & Hersh, L. B. (2012). Degradation of islet amyloid polypeptide by neprilysin. Diabetologia, 55, 2989–2998. https://doi.org/10.1007/s00125-012-2678-y
- Hama, E., Shirotani, K., Masumoto, H., Sekine-Aizawa, Y., Aizawa, H., & Saido, T. C. (2001). Clearance of extracellular and cell-associated amyloid beta peptide through viral expression of neprilysin in primary neurons. Journal of Biochemistry, 130, 721–726. https://doi.org/10.1093/oxfordjournals.jbchem.a003040
- Hardy, J., & Selkoe, D. J. (2002). The amyloid hypothesis of Alzheimer's disease: Progress and problems on the road to therapeutics. Science, 297, 353–356. https://doi.org/10.1126/science.1072994
- Hoshiba, T., Lu, H., Yamada, T., Kawazoe, N., Tateishi, T., & Chen, G. (2011). Effects of extracellular matrices derived from different cell sources on chondrocyte functions. Biotechnology Progress, 27, 788–795. https://doi.org/10.1002/btpr.592
- Hunsberger, J. G., Rao, M., Kurtzberg, J., Bulte, J. W. M., Atala, A., LaFerla, F. M., … Doraiswamy, P. M. (2016). Accelerating stem cell trials for Alzheimer's disease. Lancet Neurology, 15, 219–230. https://doi.org/10.1016/s1474-4422(15)00332-4
- Kang, Q., Xiang, Y., Li, D., Liang, J., Zhang, X., Zhou, F., … Li, Y. (2017). Mir-124-3p attenuates hyperphosphorylation of tau protein-induced apoptosis via caveolin-1-pi3k/akt/gsk3beta pathway in n2a/APP695swe cells. Oncotarget, 8, 24314–24326. https://doi.org/10.18632/oncotarget.15149
- Kang, Y., Kim, S., Bishop, J., Khademhosseini, A., & Yang, Y. (2012). The osteogenic differentiation of human bone marrow MSCs on HUVEC-derived ECM and beta-TCP scaffold. Biomaterials, 33, 6998–7007. https://doi.org/10.1016/j.biomaterials.2012.06.061
- Kim, J., Kleizen, B., Choy, R., Thinakaran, G., Sisodia, S. S., & Schekman, R. W. (2007). Biogenesis of gamma-secretase early in the secretory pathway. The Journal of Cell Biology, 179, 951–963. https://doi.org/10.1083/jcb.200709012
- Kim, Y. H., Choi, S. H., D'Avanzo, C., Hebisch, M., Sliwinski, C., Bylykbashi, E., … Kim, D. Y. (2015). A 3D human neural cell culture system for modeling Alzheimer's disease. Nature Protocols, 10, 985–1006. https://doi.org/10.1038/nprot.2015.065
- Kolarova, M., Garcia-Sierra, F., Bartos, A., Ricny, J., & Ripova, D. (2012). Structure and pathology of tau protein in Alzheimer disease. International Journal of Alzheimer's Disease, 2012, 731526. https://doi.org/10.1155/2012/731526
- Lee, H. K., Velazquez Sanchez, C., Chen, M., Morin, P. J., Wells, J. M., Hanlon, E. B., & Xia, W. (2016). Three dimensional human neuro-spheroid model of Alzheimer's disease based on differentiated induced pluripotent stem cells. PLoS ONE, 11, e0163072. https://doi.org/10.1371/journal.pone.0163072
- Leissring, M. A., Farris, W., Chang, A. Y., Walsh, D. M., Wu, X., Sun, X., … Selkoe, D. J. (2003). Enhanced proteolysis of beta-amyloid in APP transgenic mice prevents plaque formation, secondary pathology, and premature death. Neuron, 40, 1087–1093. https://doi.org/10.1016/S0896-6273(03)00787-6
- Li, X., Han, J., Zhao, Y., Ding, W., Wei, J., Han, S., … Dai, J. (2015). Functionalized collagen scaffold neutralizing the myelin-inhibitory molecules promoted neurites outgrowth in vitro and facilitated spinal cord regeneration in vivo. ACS Applied Materials & Interfaces, 7, 13960–13971. https://doi.org/10.1021/acsami.5b03879
- Lin, H., Yang, G., Tan, J., & Tuan, R. S. (2012). Influence of decellularized matrix derived from human mesenchymal stem cells on their proliferation, migration and multi-lineage differentiation potential. Biomaterials, 33, 4480–4489. https://doi.org/10.1016/j.biomaterials.2012.03.012
- Marr, R. A., Rockenstein, E., Mukherjee, A., Kindy, M. S., Hersh, L. B., Gage, F. H., … Masliah, E. (2003). Neprilysin gene transfer reduces human amyloid pathology in transgenic mice. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 23, 1992–1996. https://doi.org/10.1523/JNEUROSCI.23-06-01992.2003
- Martino, M. M., Briquez, P. S., Guc, E., Tortelli, F., Kilarski, W. W., Metzger, S., … Hubbell, J. A. (2014). Growth factors engineered for super-affinity to the extracellular matrix enhance tissue healing. Science, 343, 885–888. https://doi.org/10.1126/science.1247663
- Mattsson, N., Rajendran, L., Zetterberg, H., Gustavsson, M., Andreasson, U., Olsson, M., … Portelius, E. (2012). BACE1 inhibition induces a specific cerebrospinal fluid beta-amyloid pattern that identifies drug effects in the central nervous system. PLoS ONE, 7, e31084. https://doi.org/10.1371/journal.pone.0031084
- Miners, J. S., Baig, S., Palmer, J., Palmer, L. E., Kehoe, P. G., & Love, S. (2008). Abeta-degrading enzymes in Alzheimer's disease. Brain Pathology, 18, 240–252. https://doi.org/10.1111/j.1750-3639.2008.00132.x
- Miners, J. S., Barua, N., Kehoe, P. G., Gill, S., & Love, S. (2011). Abeta-degrading enzymes: Potential for treatment of Alzheimer disease. Journal of Neuropathology and Experimental Neurology, 70, 944–959. https://doi.org/10.1097/NEN.0b013e3182345e46
- Miners, J. S., Kehoe, P. G., & Love, S. (2008). Immunocapture-based fluorometric assay for the measurement of insulin-degrading enzyme activity in brain tissue homogenates. Journal of Neuroscience Methods, 169, 177–181. https://doi.org/10.1016/j.jneumeth.2007.12.003
- Moore, A. M., MacEwan, M., Santosa, K. B., Chenard, K. E., Ray, W. Z., Hunter, D. A., … Johnson, P. J. (2011). Acellular nerve allografts in peripheral nerve regeneration: A comparative study. Muscle & Nerve, 44, 221–234. https://doi.org/10.1002/mus.22033
- Moussa, C. E. (2017). Beta-secretase inhibitors in phase I and phase II clinical trials for Alzheimer's disease. Expert Opinion on Investigational Drugs, 26, 1131–1136. https://doi.org/10.1080/13543784.2017.1369527
- Park, M. H., Lee, J. K., Choi, S., Ahn, J., Jin, H. K., Park, J. S., & Bae, J. S. (2013). Recombinant soluble neprilysin reduces amyloid-beta accumulation and improves memory impairment in Alzheimer's disease mice. Brain Research, 1529, 113–124. https://doi.org/10.1016/j.brainres.2013.05.045
- Schlie-Wolter, S., Ngezahayo, A., & Chichkov, B. N. (2013). The selective role of ECM components on cell adhesion, morphology, proliferation and communication in vitro. Experimental Cell Research, 319, 1553–1561. https://doi.org/10.1016/j.yexcr.2013.03.016
- Shakouri-Motlagh, A., O'Connor, A. J., Brennecke, S. P., Kalionis, B., & Heath, D. E. (2017). Native and solubilized decellularized extracellular matrix: A critical assessment of their potential for improving the expansion of mesenchymal stem cells. Acta Biomaterialia, 55, 1–12. https://doi.org/10.1016/j.actbio.2017.04.014
- Singelyn, J. M., Sundaramurthy, P., Johnson, T. D., Schup-Magoffin, P. J., Hu, D. P., Faulk, D. M., … Christman, K. L. (2012). Catheter-deliverable hydrogel derived from decellularized ventricular extracellular matrix increases endogenous cardiomyocytes and preserves cardiac function post-myocardial infarction. Journal of the American College of Cardiology, 59, 751–763. https://doi.org/10.1016/j.jacc.2011.10.888
- Sonnenberg, S. B., Rane, A. A., Liu, C. J., Rao, N., Agmon, G., Suarez, S., … Christman, K. L. (2015). Delivery of an engineered HGF fragment in an extracellular matrix-derived hydrogel prevents negative LV remodeling post-myocardial infarction. Biomaterials, 45, 56–63. https://doi.org/10.1016/j.biomaterials.2014.12.021
- Sun, J., Zhao, Y., Li, Q., Chen, B., Hou, X., Xiao, Z., & Dai, J. (2016). Controlled release of collagen-binding SDF-1α improves cardiac function after myocardial infarction by recruiting endogenous stem cells. Scientific Reports, 6, 26683. https://doi.org/10.1038/srep26683
- Sun, X. J., Chen, W. D., & Wang, Y. D. (2015). Beta-amyloid: The key peptide in the pathogenesis of Alzheimer's disease. Frontiers in Pharmacology, 6, 221. https://doi.org/10.3389/fphar.2015.00221
- Takahashi, R. H., Nagao, T., & Gouras, G. K. (2017). Plaque formation and the intraneuronal accumulation of beta-amyloid in Alzheimer's disease. Pathology International, 67, 185–193. https://doi.org/10.1111/pin.12520
- Zhang, Y., McLaughlin, R., Goodyer, C., & LeBlanc, A. (2002). Selective cytotoxicity of intracellular amyloid beta peptide1-42 through p53 and Bax in cultured primary human neurons. The Journal of Cell Biology, 156, 519–529. https://doi.org/10.1083/jcb.200110119
- Zheng, W. H., Bastianetto, S., Mennicken, F., Ma, W., & Kar, S. (2002). Amyloid beta peptide induces tau phosphorylation and loss of cholinergic neurons in rat primary septal cultures. Neuroscience, 115, 201–211. https://doi.org/10.1016/S0306-4522(02)00404-9
- Zhou, Y., Xu, Z., Quan, D., Zhang, F., Zhang, H., Xiao, T., … Suo, G. (2018). Nuclear respiratory factor 1 promotes spheroid survival and mesenchymal transition in mammary epithelial cells. Oncogene, 37, 6152–6165. https://doi.org/10.1038/s41388-018-0349-2
