Neural Progenitor Cells Promote Axonal Growth and ...

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Research Article: New Research | Development

Neural Progenitor Cells Promote Axonal Growth and Alter Axonal mRNA Localization in Adult Neurons Neural progenitors alter axonal mRNA transport Tanuja T. Merianda1, Ying Jin1, Ashley L. Kalinski2, Pabitra K. Sahoo2, Itzhak Fischer1 and Jeffery L. Twiss2 1

Department of Anatomy and Neurobiology, Drexel University College of Medicine, Philadelphia, PA, USA

2

Department of Biological Sciences, University of South Carolina, Columbia, SC, USA

DOI: 10.1523/ENEURO.0171-16.2017 Received: 18 June 2016 Revised: 13 January 2017 Accepted: 13 January 2017 Published: 24 January 2017

Author Contributions: TTM, YJ, ALK, and PKS performed research. TTM, YJ, PKS, IF, and JLT designed experiments. TTM, IF, and JLT wrote manuscript. Funding: NIH/NINDS P01-NS055976

Conflict of Interest: Authors report no conflict of interest. This work was supported by grants from the National Institutes of Health (P01-NS055976 to IF and JLT). JLT is the incumbent South Carolina SmartState Chair in Childhood Neurotherapeutics at Univ. South Carolina. Correspondence should be addressed to Jeffery L. Twiss, Dept Biological Sciences, University of South Carolina, 715 Sumter Street, CLS 705/707, Columbia, SC 29208, E-mail: [email protected] Cite as: eNeuro 2017; 10.1523/ENEURO.0171-16.2017 Alerts: Sign up at eneuro.org/alerts to receive customized email alerts when the fully formatted version of this article is published.

Accepted manuscripts are peer-reviewed but have not been through the copyediting, formatting, or proofreading process. This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed. Copyright © 2017 the authors

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ƉƌŝŽƌƚŽĨƌĞĞnjŝŶŐŽĨĐƵůƚƵƌĞƐĂƚϮпϭϬϲĐĞůůƐͬŵůŝŶĨƌĞĞnjŝŶŐŵĞĚŝƵŵ;ϴϬй'ZWďĂƐĂůŵĞĚŝƵŵƐƵƉƉůĞŵĞŶƚĞĚ

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ĞdžƉĞƌŝŵĞŶƚƐ͕'ZWĂŶĚ'ZWͬEZWĐĞůůƐǁĞƌĞƵƐĞĚďLJƚŚĞƚŚŝƌĚƉĂƐƐĂŐĞ͘

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ƵůƚƵƌĞƐŽĨĞŵďƌLJŽŶŝĐƌĂƚ'ZWƐĂŶĚŵŝdžĞĚ'ZWͬEZWƐǁĞƌĞŐĞŶĞƌĂƚĞĚĨƌŽŵĨƌŽnjĞŶĂůŝƋƵŽƚƐĂƐ

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ƉƌĞǀŝŽƵƐůLJĚĞƐĐƌŝďĞĚ;,ĂĂƐĞƚĂů͕͘ϮϬϭϮ͖,ĂLJĂŬĂǁĂĞƚĂů͕͘ϮϬϭϱͿ͘'ZWŽƌ'ZWͬEZWĐĞůůŵŝdžƚƵƌĞƐǁĞƌĞ

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ď&'&ĨŽƌĞdžƉĂŶƐŝŽŶ͘ƚůĞĂƐƚϮϰŚƌ͘ƉƌŝŽƌƚŽĞdžƉĞƌŝŵĞŶƚƐĨŽƌĐŽͲĐƵůƚƵƌĞŽƌĐŽůůĞĐƚŝŶŐĐŽŶĚŝƚŝŽŶĞĚ

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ƚƌŝƚƵƌĂƚŝŽŶ͕Z'ƐǁĞƌĞƉĞůůĞƚĞĚĂƚϭϬϬdžŐĨŽƌϮϬŵŝŶ͘ĂŶĚƚŚĞŶǁĂƐŚĞĚǁŝƚŚDDͬ&ϭϮƐƵƉƉůĞŵĞŶƚĞĚ

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ǁŝƚŚϭϱй^͘ĨƚĞƌϮĂĚĚŝƚŝŽŶĂůǁĂƐŚĞƐ͕ĚŝƐƐŽĐŝĂƚĞĚŐĂŶŐůŝĂǁĞƌĞƉůĂƚĞĚĐŽĂƚĞĚŐůĂƐƐĐŽǀĞƌƐůŝƉƐ͘&Žƌ

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'ZWŵĞĚŝƵŵ;ď&'&ĂŶĚEdϯĞdžĐůƵĚĞĚͿĂŶĚĐƵůƚƵƌĞƐǁĞƌĞŝŶĐƵďĂƚĞĚĂƚϯϳΣ͕ϱйKϮ͘&ŽƌĂŶĂůLJƐĞƐŽĨ

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ƚŚĂƚŚĂĚďĞĞŶƐŝŵŝůĂƌůLJŝŶĐƵďĂƚĞĚĂƚϯϳ°͕ϱйKϮĨŽƌĞƋƵŝǀĂůĞŶƚĚƵƌĂƚŝŽŶ͘

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ĂdžŽŶĂůZEĨƌŽŵƵƉƉĞƌĂŶĚůŽǁĞƌŵĞŵďƌĂŶĞƐƵƌĨĂĐĞƐĂĨƚĞƌϯĚĂLJƐĞdžƉŽƐƵƌĞƚŽƉƌŽŐĞŶŝƚŽƌĐĞůůƐ;ϲ/s

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ƚŽƚĂůͿ͘

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WůĂƐŵŝĚƐ͕sŝƌĂůWƌĞƉĂƌĂƚŝŽŶƐ͕ĂŶĚdƌĂŶƐĨĞĐƚŝŽŶƐʹŝĨĨƵƐŝŽŶůŝŵŝƚĞĚĞ'&WDzZƌĞƉŽƌƚĞƌĐŽŶƐƚƌƵĐƚǁŝƚŚ

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ϱ͛hdZŽĨĂŵ'ŝŽ^ĞĂƌĐŚdĞĐŚŶŽůŽŐŝĞƐ͘

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ǁĂƐŚĞƐ͕ĂŶĚ/&ǁĞƌĞƉĞƌĨŽƌŵĞĚĂƐĚĞƐĐƌŝďĞĚ;^ƉŝůůĂŶĞĞƚĂů͕͘ϮϬϭϯͿ͘WƌŝŵĂƌLJĂŶƚŝďŽĚŝĞƐĐŽŶƐŝƐƚĞĚŽĨĂ

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&/^,ĂƐĚĞƐĐƌŝďĞĚ;DĞƌŝĂŶĚĂĞƚĂů͕͘ϮϬϭϯͿ͘^ĞŶƐĞĂŶĚĂŶƚŝƐĞŶƐĞĐZEƉƌŽďĞƐǁĞƌĞŐĞŶĞƌĂƚĞĚďLJŝŶǀŝƚƌŽ

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;ϭ͗ϱϬϬ͖DŝůůŝƉŽƌĞͿĨŽůůŽǁĞĚďLJDͲĐŽŶũƵŐĂƚĞĚŐŽĂƚĂŶƚŝͲƌĂďďŝƚ;ϭ͗ϰϬϬ͖:ĂĐŬƐŽŶ/ŵŵƵŶŽZĞƐ͘ͿĂŶĚLJϯͲ

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ĐŽŶũƵŐĂƚĞĚŵŽƵƐĞĂŶƚŝͲĚŝŐŽdžŝŐĞŶŝŶĂŶƚŝďŽĚŝĞƐ;ϭ͗ϮϬϬ͖:ĂĐŬƐŽŶ/ŵŵƵŶŽZĞƐ͘Ϳ͘ŽǀĞƌƐůŝƉƐĨŽƌďŽƚŚ

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^ƚĞůůĂƌŝƐΠĂŶĚĐZEƉƌŽďĞ&/^,ͬ/&ǁĞƌĞŵŽƵŶƚĞĚǁŝƚŚWƌŽůŽŶŐ'ŽůĚŶƚŝĨĂĚĞ;/ŶǀŝƚƌŽŐĞŶͿ͘ZEƐŝŐŶĂů

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EĞƵƌĂůƉƌŽŐĞŶŝƚŽƌƐĂůƚĞƌĂdžŽŶĂůŵZEƚƌĂŶƐƉŽƌƚ

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ϯƐĞƉĂƌĂƚĞƚƌĂŶƐĨĞĐƚŝŽŶĞdžƉĞƌŝŵĞŶƚƐ͘

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:ĂĐŬƐŽŶ/ŵŵƵŶŽZĞƐ͘Ϳ͘&ŽƌƐƚĂŝŶŝŶŐƌĂƚƉƌŽŐĞŶŝƚŽƌĐĞůůƐĐŽͲĐƵůƚƵƌĞĚǁŝƚŚĞdžƉůĂŶƚZ'Ɛ͕ƚŚĞ'ZWͬEZWƐŽŶ

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;DŽůĞĐƵůĂƌWƌŽďĞƐͿ͘

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ďŽĚLJďLJĂƚůĞĂƐƚϰϬϬђŵ͘

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ƚŚŝƐ͕ƚŚĞWdŵĞŵďƌĂŶĞǁŝƚŚĞdžƉůĂŶƚƐǁĂƐĞdžĐŝƐĞĚĂĨƚĞƌ/&ĂŶĚŝŵĂŐĞĚŝŶƉŚŽƐƉŚĂƚĞďƵĨĨĞƌĞĚƐĂůŝŶĞ

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'ZWͬEZWǁĞƌĞŝŵĂŐĞĚƐĞƉĂƌĂƚĞůLJ͘

ʹͷͻ

džŽŶŽƵƚŐƌŽǁƚŚĂƐƐĂLJƐʹEĞƵƌŝƚĞŽƵƚŐƌŽǁƚŚĨƌŽŵZ'Ͳ'ZWĂŶĚZ'Ͳ'ZWͬEZWĐŽͲĐƵůƚƵƌĞƐĂŶĚZ'Ɛ

ʹ͸Ͳ

ƚƌĞĂƚĞĚǁŝƚŚĐŽŶĚŝƚŝŽŶĞĚŵĞĚŝƵŵǁĂƐĂŶĂůLJnjĞĚĨƌŽŵƌĂŶĚŽŵŝŵĂŐĞƐŽĨβ///ͲƚƵďƵůŝŶŝŵŵƵŶŽƐƚĂŝŶĞĚ

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ĐŽǀĞƌƐůŝƉƐ͘>ĞŶŐƚŚŽĨůŽŶŐĞƐƚĂdžŽŶŽĨŝŶĚŝǀŝĚƵĂůŝŵĂŐĞƐǁĂƐŵĞĂƐƵƌĞĚďLJƵƐŝŶŐ/ŵĂŐĞ:ĂƐĚĞƐĐƌŝďĞĚ

WĂŐĞϭϭŽĨϯϬ

EĞƵƌĂůƉƌŽŐĞŶŝƚŽƌƐĂůƚĞƌĂdžŽŶĂůŵZEƚƌĂŶƐƉŽƌƚ

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;ŽŶŶĞůůLJĞƚĂů͕͘ϮϬϭϭͿ͘&ŽƌĚŝƐƐŽĐŝĂƚĞĚZ'ƐƉůĂƚĞĚŽŶĐŽǀĞƌƐůŝƉƐŽǀĞƌďĞĚŽĨ'ZWͬEZWƐ͕ŶĞƵƌŝƚĞŐƌŽǁƚŚ

ʹ͸͵

ǁĂƐĂŶĂůLJnjĞĚƵƐŝŶŐt/^ͲEĞƵƌŽŵĂƚŚƐŽĨƚǁĂƌĞƉĂĐŬĂŐĞ;ZŝƐŚĂůĞƚĂů͕͘ϮϬϭϯͿĨƌŽŵĐƵůƚƵƌĞƐƐƚĂŝŶĞĚĨŽƌE&>͕

ʹ͸Ͷ

E&DĂŶĚE&,͘&ŽƌƚŚŝƐ͕ĂŶĂƵƚŽŵĂƚĞĚƐƚĂŐĞǁĂƐƵƐĞĚƚŽĐĂƉƚƵƌĞĂůůŶĞƵƌŽŶƐŽŶϭϮŵŵĐŽǀĞƌƐůŝƉĨŽƌ

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ĂŶĂůLJƐĞƐ͘ƚůĞĂƐƚƚŚƌĞĞƐĞƉĂƌĂƚĞĐƵůƚƵƌĞƉƌĞƉĂƌĂƚŝŽŶƐǁĞƌĞĂŶĂůLJnjĞĚĨŽƌĞĂĐŚĐŽŶĚŝƚŝŽŶ͘

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^ƚĂƚŝƐƚŝĐĂůĂŶĂůLJƐĞƐʹWƌŝƐŵϰƐŽĨƚǁĂƌĞƉĂĐŬĂŐĞ;'ƌĂƉŚWĂĚͿǁĂƐƵƐĞĚĨŽƌĂůůƐƚĂƚŝƐƚŝĐĂůĂŶĂůLJƐĞƐ͘

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^ƚƵĚĞŶƚ͛ƐƚͲƚĞƐƚǁĂƐƵƐĞĚƚŽĐŽŵƉĂƌĞƚǁŽŵĞĂŶƐŽĨŝŶĚĞƉĞŶĚĞŶƚŐƌŽƵƉƐŝŶƚŚĞĂdžŽŶĂůŐƌŽǁƚŚĂƐƐĂLJƐ

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ĂŶĚĨůƵŽƌĞƐĐĞŶƚŝŶƚĞŶƐŝƚLJĐŽŵƉĂƌŝƐŽŶƐĨƌŽŵ&/^,ͬ/&ŝŵĂŐĞƐ͘

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'ůŝĂůƌĞƐƚƌŝĐƚĞĚƉƌŽŐĞŶŝƚŽƌĐĞůůƐŝŶĐƌĞĂƐĞŶĞƵƌŝƚĞŽƵƚŐƌŽǁƚŚĨƌŽŵĂĚƵůƚZ'ŶĞƵƌŽŶƐ͘

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dƌĂŶƐƉůĂŶƚŽĨEWĚĞƌŝǀĞĚĨƌŽŵĞŵďƌLJŽŶŝĐƐƉŝŶĂůĐŽƌĚƐƵƉƉŽƌƚƐŐƌŽǁƚŚŽĨŚŽƐƚƐĞŶƐŽƌLJĂdžŽŶƐ

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ŝŶƚŽƚŚĞŐƌĂĨƚĞĚƉƌŽŐĞŶŝƚŽƌĐĞůůƐĨŽůůŽǁŝŶŐƐƉŝŶĂůĐŽƌĚŝŶũƵƌLJ;ŽŶŶĞƌĞƚĂů͕͘ϮϬϭϬ͖ŽŶŶĞƌĞƚĂů͕͘ϮϬϭϭ͖>Ƶ

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ĞƚĂů͕͘ϮϬϭϮͿ͘ŽŶĚŝƚŝŽŶĞĚŵĞĚŝƵŵĨƌŽŵŚŝŐŚͲĚĞŶƐŝƚLJďƵƚŶŽƚůŽǁĚĞŶƐŝƚLJ'ZWĐƵůƚƵƌĞƐǁĂƐĂůƐŽƐŚŽǁŶ

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ƚŽŝŶĐƌĞĂƐĞĂďŝůŝƚLJŽĨĂdžŽŶƐƚŽŐƌŽǁŝŶƚŽŶŽŶͲƉĞƌŵŝƐƐŝǀĞĐŚŽŶĚƌŽŝƚŝŶƐƵůĨĂƚĞƉƌŽƚĞŽŐůLJĐĂŶ;^W'Ϳ

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ƐƵďƐƚƌĂƚĞƐ͕ďŽƚŚĨŽƌĞŵďƌLJŽŶŝĐĐŚŝĐŬĂŶĚƌĂƚZ'Ɛ;ĞǀĞůƐŽĨ'WͲϰϯ͕/ŵƉŽƌƚŝŶβϭ͕ĂŶĚEĞƵƌŝƚŝŶŵZEƐŝŶĐƌĞĂƐĞĚŝŶƚŚĞĂdžŽŶƐĐŽͲ

͵͸ͳ

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͵͸ʹ

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͵͸͵

ƚŚĞZ'ƐĐŽͲĐƵůƚƵƌĞĚǁŝƚŚ'ZWͬEZWƐ;&ŝŐƵƌĞϰͿ͕ǁĂƐŝŶĐƌĞĂƐĞĚŝŶƚŚĞĂdžŽŶĂůĐŽŵƉĂƌƚŵĞŶƚ;&ŝŐƵƌĞϰͿ͘

͵͸Ͷ

&ŝŶĂůůLJƚŚĞƐĞĐŚĂŶŐĞƐǁĞƌĞŶŽƚƵŶŝǀĞƌƐĂů͕ŝŶƚŚĂƚZĞŐϯĂŵZEǁĂƐŶŽƚĚĞƚĞĐƚĞĚŝŶƚŚĞĂdžŽŶƐLJĞƚŝƚǁĂƐ

͵͸ͷ

ĐůĞĂƌůLJĂŵƉůŝĨŝĞĚĨƌŽŵƚŚĞĐĞůůďŽĚLJĐŽŵƉĂƌƚŵĞŶƚƐŽĨďŽƚŚƚŚĞĐŽŶƚƌŽůZ'ƐĂŶĚZ'ƐĐŽͲĐƵůƚƵƌĞĚǁŝƚŚ

͵͸͸

'ZWͬEZWƐ;&ŝŐƵƌĞϰͲͿ͘dƌĂŶƐĐƌŝƉƚŝŽŶĂůŝŶĐƌĞĂƐĞƐŽĨZĞŐϯĂŶĚ,DWŵZEƐǁĞƌĞƉƌĞǀŝŽƵƐůLJƐŚŽǁŶ

͵͸͹

ŝŶ>ϰͲϱZ'ƐĨŽůůŽǁŝŶŐĂŶŝŶǀŝǀŽƐĐŝĂƚŝĐŶĞƌǀĞĐƌƵƐŚ͕ĂŶĚďŽƚŚŵZEƐƐŚŽǁŝŶĐƌĞĂƐĞĚůŽĐĂůŝnjĂƚŝŽŶƚŽ

͵͸ͺ

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Ͷͷ͵

EĞƵƌŽŶĂůZĞŐϯŵZEǁĂƐŶŽƚƐŝŐŶŝĨŝĐĂŶƚůLJĐŚĂŶŐĞĚĂŶĚ,DWŵZEƐŚŽǁĞĚĂƐŝŐŶŝĨŝĐĂŶƚĚĞĐƌĞĂƐĞŝŶ

ͶͷͶ

ƚŚĞŶĂŢǀĞZ'Ͳ'ZWͬEZWĐŽͲĐƵůƚƵƌĞ;&ŝŐƵƌĞϰͿ͕ǁŚŝůĞƚŚĞƐĞŵZEƐŝŶĐƌĞĂƐĞďLJΕϳĂŶĚΕϭϴϬϬĨŽůĚ͕

Ͷͷͷ

ƌĞƐƉĞĐƚŝǀĞůLJ͕ŝŶ>ϰͲϱZ'ƐĂĨƚĞƌƐĐŝĂƚŝĐŶĞƌǀĞĐƌƵƐŚ;ϰͲϱZ'Ɛ;ďLJΕϱĂŶĚΕϭϱĨŽůĚ͕ƌĞƐƉĞĐƚŝǀĞůLJͿĨŽůůŽǁŝŶŐƐĐŝĂƚŝĐŶĞƌǀĞĐƌƵƐŚŝŶũƵƌLJ

Ͷͷ͹

;ƵY͕&ůĂŶĂŐĂŶ:';ϮϬϬϮͿdžŽŶĂůƉƌŽƚĞŝŶƐLJŶƚŚĞƐŝƐƉƌŽǀŝĚĞƐĂŵĞĐŚĂŶŝƐŵĨŽƌůŽĐĂůŝnjĞĚ ƌĞŐƵůĂƚŝŽŶĂƚĂŶŝŶƚĞƌŵĞĚŝĂƚĞƚĂƌŐĞƚ͘ĞůůϭϭϬ͗ϮϮϯͲϮϯϱ͘

ͷͶ͹ ͷͶͺ

ŚĂŶĚƌĂŶsĞƚĂů͘;ϮϬϭϲͿ^LJƐƚĞŵƐͲ>ĞǀĞůŶĂůLJƐŝƐŽĨƚŚĞWĞƌŝƉŚĞƌĂůEĞƌǀĞ/ŶƚƌŝŶƐŝĐdžŽŶĂů'ƌŽǁƚŚ WƌŽŐƌĂŵ͘EĞƵƌŽŶϴϵ͗ϵϱϲͲϵϳϬ͘

ͷͶͻ ͷͷͲ

ŽůĂŬ͕:ŝ^:͕WŽƌƐĞd͕:ĂĨĨƌĞLJ^Z;ϮϬϭϯͿZĞŐƵůĂƚŝŽŶŽĨĂdžŽŶŐƵŝĚĂŶĐĞďLJĐŽŵƉĂƌƚŵĞŶƚĂůŝnjĞĚŶŽŶƐĞŶƐĞͲ ŵĞĚŝĂƚĞĚŵZEĚĞĐĂLJ͘Ğůůϭϱϯ͗ϭϮϱϮͲϭϮϲϱ͘

ͷͷͳ ͷͷʹ ͷͷ͵

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ͷ͸Ͳ ͷ͸ͳ

ƵůŝŶ:E͕>ƵW;ϮϬϭϰͿƌŝĚŐŝŶŐƚŚĞŝŶũƵƌĞĚƐƉŝŶĂůĐŽƌĚǁŝƚŚŶĞƵƌĂůƐƚĞŵĐĞůůƐ͘EĞƵƌĂůZĞŐĞŶZĞƐϵ͗ϮϮϵͲ Ϯϯϭ͘

ͷ͸ʹ ͷ͸͵ ͷ͸Ͷ

Žŵd͕ŶƚĂƌ>E͕^ŝŶŐĞƌZ,͕ĂƐƐĞůů':;ϮϬϬϯͿ>ŽĐĂůŝnjĂƚŝŽŶŽĨĂďĞƚĂͲĂĐƚŝŶŵĞƐƐĞŶŐĞƌƌŝďŽŶƵĐůĞŽƉƌŽƚĞŝŶ ĐŽŵƉůĞdžǁŝƚŚnjŝƉĐŽĚĞͲďŝŶĚŝŶŐƉƌŽƚĞŝŶŵŽĚƵůĂƚĞƐƚŚĞĚĞŶƐŝƚLJŽĨĚĞŶĚƌŝƚŝĐĨŝůŽƉŽĚŝĂĂŶĚĨŝůŽƉŽĚŝĂů ƐLJŶĂƉƐĞƐ͘:EĞƵƌŽƐĐŝϮϯ͗ϭϬϰϯϯͲϭϬϰϰϰ͘

ͷ͸ͷ ͷ͸͸ ͷ͸͹

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ͷ͸ͺ ͷ͸ͻ

'ŽŵĞƐ͕DĞƌŝĂŶĚĂdd͕>ĞĞ^:͕zŽŽ^͕dǁŝƐƐ:>;ϮϬϭϰͿDŽůĞĐƵůĂƌĚĞƚĞƌŵŝŶĂŶƚƐŽĨƚŚĞĂdžŽŶĂůŵZE ƚƌĂŶƐĐƌŝƉƚŽŵĞ͘ĞǀĞůŽƉEĞƵƌŽďŝŽůϳϰ͗ϮϭϴͲϮϯϮ͘

ͷ͹Ͳ ͷ͹ͳ

,ĂĂƐ͕&ŝƐĐŚĞƌ/;ϮϬϭϰͿdƌĂŶƐƉůĂŶƚŝŶŐŶĞƵƌĂůƉƌŽŐĞŶŝƚŽƌƐƚŽďƵŝůĚĂŶĞƵƌŽŶĂůƌĞůĂLJĂĐƌŽƐƐƚŚĞŝŶũƵƌĞĚ ƐƉŝŶĂůĐŽƌĚ͘EĞƵƌĂůZĞŐĞŶZĞƐϵ͗ϭϭϳϯͲϭϭϳϲ͘

ͷ͹ʹ ͷ͹͵

,ĂĂƐ͕EĞƵŚƵďĞƌ͕zĂŵĂŐĂŵŝd͕ZĂŽD͕&ŝƐĐŚĞƌ/;ϮϬϭϮͿWŚĞŶŽƚLJƉŝĐĂŶĂůLJƐŝƐŽĨĂƐƚƌŽĐLJƚĞƐĚĞƌŝǀĞĚĨƌŽŵ ŐůŝĂůƌĞƐƚƌŝĐƚĞĚƉƌĞĐƵƌƐŽƌƐĂŶĚƚŚĞŝƌŝŵƉĂĐƚŽŶĂdžŽŶƌĞŐĞŶĞƌĂƚŝŽŶ͘džƉĞƌEĞƵƌŽůϮϯϯ͗ϳϭϳͲϳϯϮ͘

WĂŐĞϮϰŽĨϯϬ

EĞƵƌĂůƉƌŽŐĞŶŝƚŽƌƐĂůƚĞƌĂdžŽŶĂůŵZEƚƌĂŶƐƉŽƌƚ

ͷ͹Ͷ ͷ͹ͷ ͷ͹͸

,ĂLJĂŬĂǁĂŽĐĂůWƌŽƚĞŝŶ ^LJŶƚŚĞƐŝƐŝŶƚŚĞdžŽŶƐŽĨZĂƚŽƌƚŝĐĂůEĞƵƌŽŶƐďLJĐƚŝǀĂƚŝŶŐɲͲŵŝŶŽͲϯͲŚLJĚƌŽdžLJͲϱͲŵĞƚŚLJůͲϰͲ ŝƐŽdžĂnjŽůĞƉƌŽƉŝŽŶŝĐĐŝĚ;DWͿZĞĐĞƉƚŽƌƐĂŶĚDĞƚĂďŽƚƌŽƉŝĐ'ůƵƚĂŵĂƚĞZĞĐĞƉƚŽƌƐ͘:ŝŽůŚĞŵ ϮϵϬ͗ϮϬϳϰϴͲϮϬϳϲϬ͘

ͷͺ͵ ͷͺͶ ͷͺͷ ͷͺ͸

:ĂďůŽŶƐŬĂ͕ƌĞůĂ͕:ĂŶŽǁƐŬŝD͕ĂůĞǁƐŬĂd͕>ƵŬŽŵƐŬĂ;ϮϬϭϱͿ^ŚŽƌƚͲ>ŝǀĞĚ ,ƵŵĂŶhŵďŝůŝĐĂůŽƌĚͲůŽŽĚͲĞƌŝǀĞĚEĞƵƌĂů^ƚĞŵĞůůƐ/ŶĨůƵĞŶĐĞƚŚĞŶĚŽŐĞŶŽƵƐ^ĞĐƌĞƚŽŵĞ ĂŶĚ/ŶĐƌĞĂƐĞƚŚĞEƵŵďĞƌŽĨŶĚŽŐĞŶŽƵƐEĞƵƌĂůWƌŽŐĞŶŝƚŽƌƐŝŶĂZĂƚDŽĚĞůŽĨ>ĂĐƵŶĂƌ^ƚƌŽŬĞ͘ DŽůĞĐEĞƵƌŽďŝŽůϱϯ͗ϲϰϭϯͲϲϰϮϱ͘

ͷͺ͹ ͷͺͺ ͷͺͻ

:ŝŶz͕EĞƵŚƵďĞƌ͕^ŝŶŐŚ͕ŽƵLJĞƌ:͕>ĞƉŽƌĞ͕ŽŶŶĞƌ:͕,ŝŵĞƐd͕ĂŵƉĂŶĞůůŝ:d͕&ŝƐĐŚĞƌ/;ϮϬϭϭͿ dƌĂŶƐƉůĂŶƚĂƚŝŽŶŽĨ,ƵŵĂŶ'ůŝĂůZĞƐƚƌŝĐƚĞĚWƌŽŐĞŶŝƚŽƌƐĂŶĚĞƌŝǀĞĚƐƚƌŽĐLJƚĞƐŝŶƚŽĂŽŶƚƵƐŝŽŶ DŽĚĞůŽĨ^ƉŝŶĂůŽƌĚ/ŶũƵƌLJ͘:EĞƵƌŽƚƌĂƵŵĂϮϴ͗ϱϳϵͲϱϵϰ͘

ͷͻͲ ͷͻͳ

:ƵŶŐ,͕KΖ,ĂƌĞD͕,Žůƚ;ϮϬϭϭͿdƌĂŶƐůĂƚŝŽŶĂůƌĞŐƵůĂƚŝŽŶŝŶŐƌŽǁƚŚĐŽŶĞƐ͘ƵƌƌKƉŝŶ'ĞŶĞƚŝĐƐĞǀĞůŽƉ Ϯϭ͗ϰϱϴͲϰϲϰ͘

ͷͻʹ ͷͻ͵ ͷͻͶ

͕^ĂĐŚĚĞǀĂZ͕'ŽŵĞƐ͕>ĞĞ^:͕^ŚĂŚ͕,ŽƵůĞ:͕dǁŝƐƐ:>;ϮϬϭϱͿŵZEƐĂŶĚWƌŽƚĞŝŶ^LJŶƚŚĞƚŝĐ DĂĐŚŝŶĞƌLJ>ŽĐĂůŝnjĞŝŶƚŽZĞŐĞŶĞƌĂƚŝŶŐ^ƉŝŶĂůŽƌĚdžŽŶƐtŚĞŶdŚĞLJƌĞWƌŽǀŝĚĞĚĂ^ƵďƐƚƌĂƚĞ dŚĂƚ^ƵƉƉŽƌƚƐ'ƌŽǁƚŚ͘:EĞƵƌŽƐĐŝϯϱ͗ϭϬϯϱϳͲϭϬϯϳϬ͘

ͷͻͷ ͷͻ͸

ĂŶĞD͕>ĞƉŽƌĞ͕&ŝƐĐŚĞƌ/;ϮϬϭϲͿ/ŵƉƌŽǀŝŶŐƚŚĞƚŚĞƌĂƉĞƵƚŝĐĞĨĨŝĐĂĐLJŽĨŶĞƵƌĂůƉƌŽŐĞŶŝƚŽƌĐĞůů ƚƌĂŶƐƉůĂŶƚĂƚŝŽŶĨŽůůŽǁŝŶŐƐƉŝŶĂůĐŽƌĚŝŶũƵƌLJ͘džƉĞƌƚZĞǀŝĞǁEĞƵƌŽƚŚĞƌŝŶƉƌĞƐƐ΀ƉƵďĂŚĞĂĚŽĨ ƉƌŝŶƚ͕K/͗ϭϬ͘ϭϬϴϬͬϭϰϳϯϳϭϳϱ͘ϮϬϭϳ͘ϭϮϳϬϮϬϲ΁

͸ͲͲ ͸Ͳͳ

>ĞƉŽƌĞ͕&ŝƐĐŚĞƌ/;ϮϬϬϱͿ>ŝŶĞĂŐĞͲƌĞƐƚƌŝĐƚĞĚŶĞƵƌĂůƉƌĞĐƵƌƐŽƌƐƐƵƌǀŝǀĞ͕ŵŝŐƌĂƚĞ͕ĂŶĚĚŝĨĨĞƌĞŶƚŝĂƚĞ ĨŽůůŽǁŝŶŐƚƌĂŶƐƉůĂŶƚĂƚŝŽŶŝŶƚŽƚŚĞŝŶũƵƌĞĚĂĚƵůƚƐƉŝŶĂůĐŽƌĚ͘džƉĞƌEĞƵƌŽůϭϵϰ͗ϮϯϬͲϮϰϮ͘

͸Ͳʹ

>ŝŵŬĞd>͕ZĂŽD^;ϮϬϬϮͿEĞƵƌĂůƐƚĞŵĐĞůůƐŝŶĂŐŝŶŐĂŶĚĚŝƐĞĂƐĞ͘:ĞůůDŽůĞĐDĞĚŝĐŝŶĞϲ͗ϰϳϱͲϰϵϲ͘

͸Ͳ͵ ͸ͲͶ

>ƵW͕͕ŚĞŶŐ͕ ŽŶŶĞƌ:D͕DĂƌƐĂůĂD͕dƵƐnjLJŶƐŬŝD,;ϮϬϭϮͿ>ŽŶŐͲĚŝƐƚĂŶĐĞŐƌŽǁƚŚĂŶĚĐŽŶŶĞĐƚŝǀŝƚLJŽĨŶĞƵƌĂů ƐƚĞŵĐĞůůƐĂĨƚĞƌƐĞǀĞƌĞƐƉŝŶĂůĐŽƌĚŝŶũƵƌLJ͘ĞůůϭϱϬ͗ϭϮϲϰͲϭϮϳϯ͘

͸Ͳͺ ͸Ͳͻ ͸ͳͲ

DĂd͕ĂƌĐŽ͕ZĂƚĂŶZZ͕tŝůůŝƐ;ϮϬϭϰͿĐDWͲƌĞƐƉŽŶƐŝǀĞĞůĞŵĞŶƚͲďŝŶĚŝŶŐƉƌŽƚĞŝŶ;ZͿĂŶĚĐDW ĐŽͲƌĞŐƵůĂƚĞĂĐƚŝǀĂƚŽƌƉƌŽƚĞŝŶϭ;WϭͿͲĚĞƉĞŶĚĞŶƚƌĞŐĞŶĞƌĂƚŝŽŶͲĂƐƐŽĐŝĂƚĞĚŐĞŶĞĞdžƉƌĞƐƐŝŽŶĂŶĚ ŶĞƵƌŝƚĞŐƌŽǁƚŚ͘:ŝŽůŚĞŵϮϴϵ͗ϯϮϵϭϰͲϯϮϵϮϱ͘

͸ͳͳ ͸ͳʹ ͸ͳ͵

DĞƌŝĂŶĚĂd͕ŽůĞŵĂŶ:͕͕^ŽƵƐĂE;ϮϬϭϱͿ DĞƐĞŶĐŚLJŵĂůƐƚĞŵĐĞůůƐƐĞĐƌĞƚŽŵĞĂƐĂŵŽĚƵůĂƚŽƌŽĨƚŚĞŶĞƵƌŽŐĞŶŝĐŶŝĐŚĞ͗ďĂƐŝĐŝŶƐŝŐŚƚƐĂŶĚ ƚŚĞƌĂƉĞƵƚŝĐŽƉƉŽƌƚƵŶŝƚŝĞƐ͘&ƌŽŶƚĞůůEĞƵƌŽƐĐŝϵ͗Ϯϰϵ͘

͸Ͷͳ ͸Ͷʹ

^ŚŽĞŵĂŬĞƌ>͕ŝĨĞ^ĐŝϳϬ͗ϯϴϳϭͲϯϴϴϮ͘

͸ͷʹ ͸ͷ͵

dƐŽ͕DĐϰŝƐƌĞƋƵŝƌĞĚĨŽƌ ƌĂƉŝĚŶĞƵƌŝƚĞĞdžƚĞŶƐŝŽŶ͘EĞƵƌŽďŝŽůŝƐϳ͗ϰϭϲͲϰϮϴ͘

͸ͷ͸ ͸ͷ͹ ͸ͷͺ

sĂŶĚĞƌĞĞ͕EŝĞůĂŶĚĞƌ,͕sŽƐ:W͕>ŽƉĞƐĚĂ^ŝůǀĂ^͕sĞƌŚĂĂŐĞŶ:͕KĞƐƚƌĞŝĐŚĞƌ͕^ĐŚƌĂŵĂ>,͕ ^ĐŚŽƚŵĂŶW͕'ŝƐƉĞŶt,;ϭϵϴϵͿdžƉƌĞƐƐŝŽŶŽĨŐƌŽǁƚŚͲĂƐƐŽĐŝĂƚĞĚƉƌŽƚĞŝŶͲϱϬ;'WϰϯͿŝŶĚŽƌƐĂů ƌŽŽƚŐĂŶŐůŝĂĂŶĚƐĐŝĂƚŝĐŶĞƌǀĞĚƵƌŝŶŐƌĞŐĞŶĞƌĂƚŝǀĞƐƉƌŽƵƚŝŶŐ͘:EĞƵƌŽƐĐŝϵ͗ϯϱϬϱͲϯϱϭϮ͘

͸ͷͻ ͸͸Ͳ ͸͸ͳ

sŝƐŚǁĂŬĂƌŵĂ^ŝ;ϮϬϭϭͿdžŽŶĂů>ŽĐĂůŝnjĂƚŝŽŶŽĨƚƌĂŶƐŐĞŶĞŵZEŝŶŵĂƚƵƌĞWE^ĂŶĚ E^ŶĞƵƌŽŶƐ͘:EĞƵƌŽƐĐŝϯϭ͗ϭϰϰϴϭͲϭϰϰϴϳ͘

͸͹͸ ͸͹͹ ͸͹ͺ

tƌŝŐŚƚ͕Žŵd͕KůĞLJŶŝŬŽǀz͕^ŚĞŶŽLJ^D͕>ŝĞďĞůƚ͕ŝĐƚĞŶďĞƌŐ:͕^ŝŶŐĞƌZ,͕ĂƐƐĞůů':;ϮϬϬϭͿ EĞƵƌŽƚƌŽƉŚŝŶͲŝŶĚƵĐĞĚƚƌĂŶƐƉŽƌƚŽĨĂďĞƚĂͲĂĐƚŝŶŵZEWĐŽŵƉůĞdžŝŶĐƌĞĂƐĞƐďĞƚĂͲĂĐƚŝŶůĞǀĞůƐĂŶĚ ƐƚŝŵƵůĂƚĞƐŐƌŽǁƚŚĐŽŶĞŵŽƚŝůŝƚLJ͘EĞƵƌŽŶϯϭ͗ϮϲϭͲϮϳϱ͘

͸ͺͺ ͸ͺͻ ͸ͻͲ

ŚĞŶŐ:ͲY͕