Downregulation of miR-204 expression defines a highly aggressive subset of Group 3/Group 4 medulloblastomas
Identifieur interne : 000517 ( Ncbi/Curation ); précédent : 000516; suivant : 000518Downregulation of miR-204 expression defines a highly aggressive subset of Group 3/Group 4 medulloblastomas
Auteurs : Harish Shrikrishna Bharambe [Inde] ; Raikamal Paul [Inde] ; Pooja Panwalkar [Inde] ; Rakesh Jalali [Inde] ; Epari Sridhar [Inde] ; Tejpal Gupta [Inde] ; Aliasgar Moiyadi [Inde] ; Prakash Shetty [Inde] ; Sadaf Kazi [Inde] ; Akash Deogharkar [Inde] ; Shalaka Masurkar [Inde] ; Kedar Yogi [Inde] ; Ratika Kunder [Inde] ; Nikhil Gadewal [Inde] ; Atul Goel [Inde] ; Naina Goel [Inde] ; Girish Chinnaswamy [Inde] ; Vijay Ramaswamy ; Neelam Vishwanath Shirsat [Inde]Source :
- Acta Neuropathologica Communications [ 2051-5960 ] ; 2019.
Abstract
Genome-wide expression profiling studies have identified four core molecular subgroups of medulloblastoma: WNT, SHH, Group 3 and Group 4. Molecular markers are necessary for accurate risk stratification in the non-WNT subgroups due to the underlying heterogeneity in genetic alterations and overall survival. MiR-204 expression was evaluated in molecularly classified 260 medulloblastomas from an Indian cohort and in 763 medulloblastomas from the MAGIC cohort, SickKids, Canada. Low expression of miR-204 in the Group 3 / Group 4 tumors identify a highly aggressive subset of tumors having poor overall survival, in the two independent cohorts of medulloblastomas. Downregulation of miR-204 expression correlates with poor survival within the Group 4 as well indicating it as a valuable risk-stratification marker in the subgroup. Restoration of miR-204 expression in multiple medulloblastoma cell lines was found to inhibit their anchorage-independent growth, invasion potential and tumorigenicity. IGF2R was identified as a novel target of miR-204. MiR-204 expression resulted in downregulation of both M6PR and IGF2R that transport lysosomal proteases from the Golgi apparatus to the lysosomes. Consistent with this finding, miR-204 expression resulted in reduction in the levels of the lysosomal proteases in medulloblastoma cells. MiR-204 expression also resulted in inhibition of autophagy that is known to be dependent on the lysosomal degradation pathway and LC3B, a known miR-204 target. Treatment with HDAC inhibitors resulted in upregulation of miR-204 expression in medulloblastoma cells, suggesting therapeutic role for these inhibitors in the treatment of medulloblastomas. In summary, miR-204 is not only a valuable risk stratification marker in the combined cohort of Group 3 / Group 4 medulloblastomas as well as in the Group 4 itself, that has paucity of good prognostication markers, but also has therapeutic potential as indicated by its tumor suppressive effect on medulloblastoma cells.
The online version of this article (10.1186/s40478-019-0697-3) contains supplementary material, which is available to authorized users.
Url:
DOI: 10.1186/s40478-019-0697-3
PubMed: 30944042
PubMed Central: 6448261
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<author><name sortKey="Bharambe, Harish Shrikrishna" sort="Bharambe, Harish Shrikrishna" uniqKey="Bharambe H" first="Harish Shrikrishna" last="Bharambe">Harish Shrikrishna Bharambe</name>
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<author><name sortKey="Panwalkar, Pooja" sort="Panwalkar, Pooja" uniqKey="Panwalkar P" first="Pooja" last="Panwalkar">Pooja Panwalkar</name>
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<author><name sortKey="Sridhar, Epari" sort="Sridhar, Epari" uniqKey="Sridhar E" first="Epari" last="Sridhar">Epari Sridhar</name>
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Parel, Mumbai, 400012 India</nlm:aff>
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</author>
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Kharghar, Navi Mumbai, 410210 India</nlm:aff>
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Parel, Mumbai, 400012 India</nlm:aff>
<country xml:lang="fr">Inde</country>
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</author>
<author><name sortKey="Shetty, Prakash" sort="Shetty, Prakash" uniqKey="Shetty P" first="Prakash" last="Shetty">Prakash Shetty</name>
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Parel, Mumbai, 400012 India</nlm:aff>
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<author><name sortKey="Kazi, Sadaf" sort="Kazi, Sadaf" uniqKey="Kazi S" first="Sadaf" last="Kazi">Sadaf Kazi</name>
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Kharghar, Navi Mumbai, 410210 India</nlm:aff>
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<author><name sortKey="Deogharkar, Akash" sort="Deogharkar, Akash" uniqKey="Deogharkar A" first="Akash" last="Deogharkar">Akash Deogharkar</name>
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Kharghar, Navi Mumbai, 410210 India</nlm:aff>
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Anushakti Nagar, Mumbai, 400085 India</nlm:aff>
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<author><name sortKey="Masurkar, Shalaka" sort="Masurkar, Shalaka" uniqKey="Masurkar S" first="Shalaka" last="Masurkar">Shalaka Masurkar</name>
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Kharghar, Navi Mumbai, 410210 India</nlm:aff>
<country xml:lang="fr">Inde</country>
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Anushakti Nagar, Mumbai, 400085 India</nlm:aff>
<country xml:lang="fr">Inde</country>
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<author><name sortKey="Yogi, Kedar" sort="Yogi, Kedar" uniqKey="Yogi K" first="Kedar" last="Yogi">Kedar Yogi</name>
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Kharghar, Navi Mumbai, 410210 India</nlm:aff>
<country xml:lang="fr">Inde</country>
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Anushakti Nagar, Mumbai, 400085 India</nlm:aff>
<country xml:lang="fr">Inde</country>
<wicri:regionArea>Anushakti Nagar, Mumbai</wicri:regionArea>
<wicri:noRegion>Mumbai</wicri:noRegion>
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</author>
<author><name sortKey="Kunder, Ratika" sort="Kunder, Ratika" uniqKey="Kunder R" first="Ratika" last="Kunder">Ratika Kunder</name>
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Kharghar, Navi Mumbai, 410210 India</nlm:aff>
<country xml:lang="fr">Inde</country>
<wicri:regionArea>Kharghar, Navi Mumbai</wicri:regionArea>
<wicri:noRegion>Navi Mumbai</wicri:noRegion>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="Aff10"><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 1775 9822</institution-id>
<institution-id institution-id-type="GRID">grid.450257.1</institution-id>
<institution>Homi Bhabha National Institute, Training School Complex,</institution>
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Anushakti Nagar, Mumbai, 400085 India</nlm:aff>
<country xml:lang="fr">Inde</country>
<wicri:regionArea>Anushakti Nagar, Mumbai</wicri:regionArea>
<wicri:noRegion>Mumbai</wicri:noRegion>
</affiliation>
</author>
<author><name sortKey="Gadewal, Nikhil" sort="Gadewal, Nikhil" uniqKey="Gadewal N" first="Nikhil" last="Gadewal">Nikhil Gadewal</name>
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<institution>Bioinformatics Centre, Advanced Centre for Treatment, Research & Education in Cancer,</institution>
<institution>Tata Memorial Centre,</institution>
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Kharghar, Navi Mumbai, 410210 India</nlm:aff>
<country xml:lang="fr">Inde</country>
<wicri:regionArea>Kharghar, Navi Mumbai</wicri:regionArea>
<wicri:noRegion>Navi Mumbai</wicri:noRegion>
</affiliation>
</author>
<author><name sortKey="Goel, Atul" sort="Goel, Atul" uniqKey="Goel A" first="Atul" last="Goel">Atul Goel</name>
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<institution-id institution-id-type="GRID">grid.414807.e</institution-id>
<institution>Department of Neurosurgery,</institution>
<institution>Seth G. S. Medical College & K. E. M. Hospital,</institution>
</institution-wrap>
Parel, Mumbai, 400012 India</nlm:aff>
<country xml:lang="fr">Inde</country>
<wicri:regionArea>Parel, Mumbai</wicri:regionArea>
<wicri:noRegion>Mumbai</wicri:noRegion>
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</author>
<author><name sortKey="Goel, Naina" sort="Goel, Naina" uniqKey="Goel N" first="Naina" last="Goel">Naina Goel</name>
<affiliation wicri:level="1"><nlm:aff id="Aff9"><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 1766 8840</institution-id>
<institution-id institution-id-type="GRID">grid.414807.e</institution-id>
<institution>Department of Pathology,</institution>
<institution>Seth G. S. Medical College & K. E. M. Hospital,</institution>
</institution-wrap>
Parel, Mumbai, 400012 India</nlm:aff>
<country xml:lang="fr">Inde</country>
<wicri:regionArea>Parel, Mumbai</wicri:regionArea>
<wicri:noRegion>Mumbai</wicri:noRegion>
</affiliation>
</author>
<author><name sortKey="Chinnaswamy, Girish" sort="Chinnaswamy, Girish" uniqKey="Chinnaswamy G" first="Girish" last="Chinnaswamy">Girish Chinnaswamy</name>
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<institution-id institution-id-type="GRID">grid.410871.b</institution-id>
<institution>Department of Medical Oncology,</institution>
<institution>Tata Memorial Hospital, Tata Memorial Centre,</institution>
</institution-wrap>
Parel, Mumbai, 400012 India</nlm:aff>
<country xml:lang="fr">Inde</country>
<wicri:regionArea>Parel, Mumbai</wicri:regionArea>
<wicri:noRegion>Mumbai</wicri:noRegion>
</affiliation>
</author>
<author><name sortKey="Ramaswamy, Vijay" sort="Ramaswamy, Vijay" uniqKey="Ramaswamy V" first="Vijay" last="Ramaswamy">Vijay Ramaswamy</name>
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<institution-id institution-id-type="GRID">grid.42327.30</institution-id>
<institution>Division of Haematology/Oncology, Department of Paediatrics,</institution>
<institution>Hospital for Sick Children and University of Toronto,</institution>
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555 University Ave, Toronto, ON M5G 1X8 Canada</nlm:aff>
<wicri:noCountry code="subfield">ON M5G 1X8 Canada</wicri:noCountry>
</affiliation>
</author>
<author><name sortKey="Shirsat, Neelam Vishwanath" sort="Shirsat, Neelam Vishwanath" uniqKey="Shirsat N" first="Neelam Vishwanath" last="Shirsat">Neelam Vishwanath Shirsat</name>
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<institution>Shirsat Laboratory, Advanced Centre for Treatment, Research & Education in Cancer,</institution>
<institution>Tata Memorial Centre,</institution>
</institution-wrap>
Kharghar, Navi Mumbai, 410210 India</nlm:aff>
<country xml:lang="fr">Inde</country>
<wicri:regionArea>Kharghar, Navi Mumbai</wicri:regionArea>
<wicri:noRegion>Navi Mumbai</wicri:noRegion>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="Aff10"><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 1775 9822</institution-id>
<institution-id institution-id-type="GRID">grid.450257.1</institution-id>
<institution>Homi Bhabha National Institute, Training School Complex,</institution>
</institution-wrap>
Anushakti Nagar, Mumbai, 400085 India</nlm:aff>
<country xml:lang="fr">Inde</country>
<wicri:regionArea>Anushakti Nagar, Mumbai</wicri:regionArea>
<wicri:noRegion>Mumbai</wicri:noRegion>
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</author>
</analytic>
<series><title level="j">Acta Neuropathologica Communications</title>
<idno type="eISSN">2051-5960</idno>
<imprint><date when="2019">2019</date>
</imprint>
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<front><div type="abstract" xml:lang="en"><p id="Par1">Genome-wide expression profiling studies have identified four core molecular subgroups of medulloblastoma: WNT, SHH, Group 3 and Group 4. Molecular markers are necessary for accurate risk stratification in the non-WNT subgroups due to the underlying heterogeneity in genetic alterations and overall survival. MiR-204 expression was evaluated in molecularly classified 260 medulloblastomas from an Indian cohort and in 763 medulloblastomas from the MAGIC cohort, SickKids, Canada. Low expression of miR-204 in the Group 3 / Group 4 tumors identify a highly aggressive subset of tumors having poor overall survival, in the two independent cohorts of medulloblastomas. Downregulation of miR-204 expression correlates with poor survival within the Group 4 as well indicating it as a valuable risk-stratification marker in the subgroup. Restoration of miR-204 expression in multiple medulloblastoma cell lines was found to inhibit their anchorage-independent growth, invasion potential and tumorigenicity. IGF2R was identified as a novel target of miR-204. MiR-204 expression resulted in downregulation of both M6PR and IGF2R that transport lysosomal proteases from the Golgi apparatus to the lysosomes. Consistent with this finding, miR-204 expression resulted in reduction in the levels of the lysosomal proteases in medulloblastoma cells. MiR-204 expression also resulted in inhibition of autophagy that is known to be dependent on the lysosomal degradation pathway and LC3B, a known miR-204 target. Treatment with HDAC inhibitors resulted in upregulation of miR-204 expression in medulloblastoma cells, suggesting therapeutic role for these inhibitors in the treatment of medulloblastomas. In summary, miR-204 is not only a valuable risk stratification marker in the combined cohort of Group 3 / Group 4 medulloblastomas as well as in the Group 4 itself, that has paucity of good prognostication markers, but also has therapeutic potential as indicated by its tumor suppressive effect on medulloblastoma cells.</p>
<sec><title>Electronic supplementary material</title>
<p>The online version of this article (10.1186/s40478-019-0697-3) contains supplementary material, which is available to authorized users.</p>
</sec>
</div>
</front>
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