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Chromogranin A regulates vesicle storage and mitochondrial dynamics to influence insulin secretion

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Abstract

Chromogranin A (CgA) is a prohormone and a granulogenic factor that regulates secretory pathways in neuroendocrine tissues. In β-cells of the endocrine pancreas, CgA is a major cargo in insulin secretory vesicles. The impact of CgA deficiency on the formation and exocytosis of insulin vesicles is yet to be investigated. In addition, no literature exists on the impact of CgA on mitochondrial function in β-cells. Using three different antibodies, we demonstrate that CgA is processed to vasostatin- and catestatin-containing fragments in pancreatic islet cells. CgA deficiency in Chga-KO islets leads to compensatory overexpression of chromogranin B, secretogranin II, SNARE proteins and insulin genes, as well as increased insulin protein content. Ultrastructural studies of pancreatic islets revealed that Chga-KO β-cells contain fewer immature secretory granules than wild-type (WT) control but increased numbers of mature secretory granules and plasma membrane-docked vesicles. Compared to WT control, CgA-deficient β-cells exhibited increases in mitochondrial volume, numerical densities and fusion, as well as increased expression of nuclear encoded genes (Ndufa9, Ndufs8, Cyc1 and Atp5o). These changes in secretory vesicles and the mitochondria likely contribute to the increased glucose-stimulated insulin secretion observed in Chga-KO mice. We conclude that CgA is an important regulator for coordination of mitochondrial dynamics, secretory vesicular quanta and GSIS for optimal secretory functioning of β-cells, suggesting a strong, CgA-dependent positive link between mitochondrial fusion and GSIS.

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Abbreviations

CgA:

Chromogranin A protein

Chga :

Mouse chromogranin A gene

Chgb :

Mouse chromogranin b gene

Gc:

Golgi complex

Gcg :

Mouse glucagon gene

Ins1 :

Mouse insulin 1 gene

Ins2 :

Mouse insulin 2 gene

ISG:

Immature secretory granule

ISGC:

ISG core

Mc:

Mitochondria

Nc:

Nucleus

MSG:

Mature secretory granule

MSGC:

MSG core

Scg2 :

Mouse secretogranin II gene

Sst :

Mouse somatostatin gene

TEM:

Transmission electron microscopy

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Acknowledgments

Transmission electron microscopy was conducted at the Cellular & Molecular Medicine Electron Microscopy Core Facility at UCSD. Mahata’s home equity loan and VMRF’s bridge funding supported this work. The Noland Scholarship from Caltech supported SM.

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    Authors and Affiliations

    1. Department of Medicine, University of California, San Diego, La Jolla, CA, USA

      Joshua Wollam, Matthew Riopel, Angelina Hernandez-Carretero, Angshuman Biswas, Gautam K. Bandyopadhyay, Nai-Wen Chi, Nicholas J. G. Webster & Sushil K. Mahata

    2. Division of Biology & Biological Engineering, California Institute of Technology, Pasadena, CA, USA

      Sumana Mahata

    3. VA San Diego Healthcare System, San Diego, CA, USA

      Nai-Wen Chi, Nicholas J. G. Webster & Sushil K. Mahata

    4. Section on Molecular Neuroscience, NIMH-IRP, Bethesda, MD, USA

      Lee E. Eiden

    5. Department of Biotechnology, Indian Institute of Technology Madras, Chennai, 600036, India

      Nitish R. Mahapatra

    6. IRCCS San Raffaele Scientific Institute, San Raffaele Vita-Salute University, Milan, Italy

      Angelo Corti

    7. Metabolic Physiology & Ultrastructural Biology Laboratory, Department of Medicine, University of California, San Diego (0732), 9500 Gilman Drive, La Jolla, CA, 92093-0732, USA

      Sushil K. Mahata

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    1. Joshua Wollam
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    Joshua Wollam and Sumana Mahata contributed equally to this work.

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    Wollam, J., Mahata, S., Riopel, M. et al. Chromogranin A regulates vesicle storage and mitochondrial dynamics to influence insulin secretion. Cell Tissue Res 368, 487–501 (2017). https://doi.org/10.1007/s00441-017-2580-5

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