Highly Cited HD Research

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In this edition of HD Insights, we take a look at impactful HD research articles of 2015. We searched Thomson Reuters’ “Web of Science” service in late 2016 to identify the five most highly cited original research articles reporting on original HD research published in 2015. We invited the corresponding authors to update us on their research and received the following responses.

Selective autophagy in HD

By: Zhenyu Yue, PhD

Highly Cited Article: Lim J, Lachenmayer ML, Wu S, et al. Proteotoxic stress induces phosphorylation of p62/SQSTM1 by ULK1 to regulate selective autophagic clearance of protein aggregates. PLoS Genet. 2015 Feb 27;11(2): e1004987.

Autophagy offers neuroprotection by the clearance of misfolded or aggregated proteins and damaged organelles; therefore, manipulating autophagy has been investigated for its potential as a therapeutic target for neurodegenerative diseases associated with protein aggregates. HD exemplifies such illness in the nervous system, as it is the result of a pathogenic polyglutamine (polyQ) expansion in the Huntingtin gene (HTT) that leads to the accumulation and aggregation of mutant huntingtin protein (mHTT) in neurons, and subsequent neurotoxicity. Enhancement of autophagy has been shown to promote the removal of mHTT and prevent neurotoxicity;1 therefore, drugs that promote autophagy pathways hold promise for the treatment of HD. However, the development of autophagy-related drugs for neurodegenerative disease has met tremendous hurdles. For example, the detailed mechanism whereby autophagy machinery selectively degrades protein aggregation is unclear. It also remains unclear exactly how and if autophagy is altered in the progression of HD. If autophagy is impaired in the diseased state, it has yet to be tested whether autophagy function is still reparable in the context of HD. Moreover, understanding autophagy in neurons has been particularly challenging, thereby hindering the effective evaluation and development of autophagy-related drugs.

Recent studies have demonstrated the selectivity of autophagy in the degradation of protein aggregates and injured organelles, which is mediated largely by the autophagy receptors, a group of proteins that recognize specific cargos or substrates and recruit them to autophagy machinery for degradation. p62/SQSTM1 is the best-characterized autophagy receptor. Studies from our group and others have found that multiple kinases, such as autophagy kinase ULK1, coordinate the phosphorylation of the p62 protein at two serine sites in the UBA domain (S405 and S409), modulating its dimerization and binding affinity to ubiquitinated cargoes, and subsequent degradation.2-4 In HD cell models and in the Q175 animal model, we find that the presence of mHTT causes a significant increase in phosphorylation of S405 and S409 in a polyQ repeat count- (cell models) and age- dependent (Q175 mice) manner. Phosphorylation of S405 and S409 also promotes the clearance of polyQ aggregates in cells upon autophagy induction. We have shown that ULK1-mediated phosphorylation of p62 does not depend on the mTOR pathway, which suggests that in addition to canonic autophagy regulation, ULK1 plays a role in autophagy cargo selection and recruitment through the receptor phosphorylation. Indeed, our study and others demonstrate that inhibition of mTOR triggers ULK1-mediated phosphorylation of ATG14 and beclin 1 that activates VPS34 lipid kinase, and increases autophagy function in canonical autophagy regulation.5,6

It is unclear why ULK1-mediated p62 phosphorylation as part of the selective autophagy response occurs late in the Q175 model (perhaps when aggregates are formed). This observation also suggests that mHTT escapes autophagic degradation at a young adult age due to lack of selective autophagy response. Using GFP-LC3 autophagy reporter mice, we examined autophagic activity in Q175 HD mice and found no evidence of autophagosome accumulation despite nuclear mHTT aggregate formation and p62 phosphorylation. Interestingly, in Q175 mouse brains, ULK1-mediated ATG14 and beclin 1 phosphorylation is decreased, accompanied by reduced VPS34 lipid kinase activity,5 which is essential for autophagy initiation. The evidence thus reveals imbalanced ULK1 kinase activity towards phosphorylation of different substrates, namely increase in p62 vs decrease in Beclin1/ATG14 complex in Q175 mice, in part due to the p62 sequestration of ULK1 kinase away from the Beclin1/ATG14 complex. Therefore, chronic p62 sequestration of ULK1 kinase caused by mHTT could be harmful to the mTOR signaling required for the activation of autophagy. This idea may explain the observation that p62 deletion partially alleviates pathological phenotypes in HD animal models.7

In summary, our data just begins to provide insights into the regulation of selective autophagy by ULK1 and p62 in HD or other proteotoxic stress conditions. We postulate that monitoring key autophagy protein phosphorylation and VPS34 activity could provide a novel way to assess in vivo autophagic activity and signaling regulation in the CNS, and under neurodegenerative conditions. Our study suggests the potential of selective autophagy signaling as novel drug targets for the treatment of HD.


1Yamamoto A, Yue Z. Autophagy and its normal and pathogenic states in the brain. Annu Rev Neurosci. 2014;37:55-78.

2Lim J, Lachenmayer ML, Wu S, et al. Proteotoxic stress induces phosphorylation of p62/SQSTM1 by ULK1 to regulate selective autophagic clearance of protein aggregates. PLoS Genet. 2015 Feb 27;11(2):e1004987.

3Matsumoto G, Wada K, Okuno M, Kurosawa M, Nukina N. Serine 403 phosphorylation of p62/SQSTM1 regulates selective autophagic clearance of ubiquitinated proteins. Mol Cell. 2011 Oct 21;44(2):279-289.

4Pilli M, Arko-Mensah J, Ponpuak M, et al. TBK-1 promotes autophagy-mediated antimicrobial defense by controlling autophagosome maturation. Immunity. 2012 Aug 2437(2):223-234.

5Wold MS, Lim J, Lachance V, et al. ULK1-mediated phosphorylation of ATG14 promotes autophagy and is impaired in Huntington’s disease models. Mol Neurodegen. 2016 Dec 9;11(1):76.

6Park JM, Jung CH, Seo M, et al. The ULK1 complex mediates MTORC1 signaling to the autophagy initiation machinery via binding and phosphorylating ATG14. Autophagy. 2016;12(3):547-564.

7Kurosawa M, Matsumoto G, Kino Y, et al. Depletion of p62 reduces nuclear inclusions and paradoxically ameliorates disease phenotypes in Huntington’s model mice. Hum Mol Genet. 2015 Feb 14;24(4):1092-1105.

Spread of Htt aggregates via phagocytosis

By: Margaret M. P. Pearce, PhD

Highly Cited Article: Pearce MMP, Spartz EJ, Hong W, Luo L, Kopito RR. Prion-like transmission of neuronal huntingtin aggregates to phagocytic glia in the Drosophila brain. Nat comm. 2015 Apr 13;6:6768.

Recent research has expanded our understanding of the essential roles played by glial cells in the development and proper functioning of the nervous system, far beyond their earlier description as cellular “glue.” Glia influence neuronal excitability, regulate neurotransmitter levels, prune excess neuronal processes during development, and clear dying neurons and toxic material from the brain. In neurodegenerative diseases, activation and recruitment of glia to regions of degeneration can be both beneficial and detrimental to neuronal survival; thus, a better understanding of glial signaling pathways that become activated in the disease state could aid the development of more successful therapies for neurodegenerative diseases.

Until recently, little was known about how glia respond to the presence of pathogenic protein aggregates in diseased brains. In this study, using the tractable model organism Drosophila, we examined whether phagocytic glia regulate the load of mutant Htt (mHtt) aggregates formed in neurons in vivo. We found that steady state numbers of mHtt aggregates in olfactory receptor neurons (ORNs) are reduced by Draper,1 a scavenger receptor expressed on the surface of all phagocytes in flies. Previous studies had identified an essential role for glial Draper in clearing degenerating axons during normal development2 or after axotomy,3 but this was the first indication that Draper-dependent phagocytosis could be linked to HD pathology.

A growing body of evidence supports prion-like spreading of protein aggregates associated with HD and other neurodegenerative diseases, whereby aggregates transfer from one cell to another, and self-replicate by seeded aggregation of natively-folded versions of the same protein. While most studies have focused on aggregate transfer between neurons, it is possible that glia also contribute to prion-like spread. For this reason, we examined whether aggregates of mHtt formed in ORNs could initiate prion-like conversion of wild-type Htt expressed in the cytoplasm of glia. Remarkably, we observed that glial wild-type Htt was converted over time into an aggregated state by mHtt aggregates formed in nearby ORN axons (Figure, part a). Since wild-type Htt only aggregates when it comes into direct physical contact with already-aggregated Htt,4,5 the appearance of punctate wild-type Htt reported entry of ORN-derived mHtt aggregate “seeds” into the glial cytoplasm.

Figure 1

Figure: Prion-like transmission of Htt aggregates from neurons to phagocytic glia in the adult Drosophila brain.

(a) Confocal images showing that wild-type HttQ25 expressed in glia (green) undergoes time-dependent conversion from soluble to aggregated (punctate) in the vicinity of mutant HttQ91 aggregates that formed in ORN axons (red). Mutant HttQ91 was expressed in DA1 ORNs, whose axons terminate in the DA1 glomerulus (DA1g, solid white line) of the antennal lobe (AL, dotted white line). Scale bars = 10μm.

(b) HttQ25 aggregate formation in the DA1 glomerulus of 7-day-old adult flies was blocked in flies homozygous for the drprΔ5 null mutation (draper -/-). Scale bars = 5μm.

(c) Model for prion-like transfer of neuronal mutant HttQ91 aggregates into the cytoplasm of glia via Draper-dependent phagocytosis. Whether ORN-derived HttQ91 aggregates escape into the glial cytoplasm during phagocytic engulfment or at a later step in phagocytosis (dotted lines) is not known.

(a and b) reproduced with permission from ref. [1].

These findings indicate that mHtt aggregates undergo prion-like transfer between the cytoplasm of neurons and glia in the intact Drosophila brain. We next took advantage of the extensive genetic toolset available in Drosophila to elucidate the mechanism responsible for neuron-to-glia Htt aggregate transfer. To our surprise, induced aggregation of glial wild-type Htt was eliminated in mutant flies that lack Draper expression (Figure, part b). In addition, RNAi-mediated knockdown of several glial genes with previously identified roles in Draper-dependent phagocytosis inhibited formation of wild-type Htt aggregates in glia. These exciting findings suggest that neuronal mHtt aggregates engulfed by Draper-dependent phagocytosis can escape from the phagolysosomal system and gain access to the glial cytoplasm (Figure, part c).

Our study suggests a double-edged role for phagocytic glia in HD pathogenesis — eliminating toxic mutant Htt aggregates from neurons, but also contributing to aggregate spread between cells. Numerous additional studies in the past few years have led to increased awareness of phagocytic glia as active players in neurodegeneration, and therefore potential therapeutic targets. In mice, the Draper homolog MEGF10 regulates turnover of synapses by phagocytic astrocytes in the adult brain,6 suggesting that protein aggregate clearance from axons might occur by a similar mechanism in mammals.  Future studies into how prion-like aggregates spread between neurons and glia, and the specific neuroprotective and neurodestructive functions of phagocytic glia will help to guide new strategies in the battle against HD and other neurodegenerative diseases.


1Pearce MMP, Spartz EJ, Hong W, Luo L, Kopito RR. Prion-like transmission of neuronal huntingtin aggregates to phagocytic glia in the Drosophila brain. Nat comm. 2015;6:6768.

2Hoopfer ED, McLaughlin T, Watts RJ, Schuldiner O, O’Leary DD, Luo L. Wlds protection distinguishes axon degeneration following injury from naturally occurring developmental pruning. Neuron. Jun 15 2006;50(6):883-895.

3MacDonald JM, Beach MG, Porpiglia E, Sheehan AE, Watts RJ, Freeman MR. The Drosophila cell corpse engulfment receptor Draper mediates glial clearance of severed axons. Neuron. Jun 15 2006;50(6):869-881.

4Chen S, Berthelier V, Yang W, Wetzel R. Polyglutamine aggregation behavior in vitro supports a recruitment mechanism of cytotoxicity. J Mol Biol. Aug 3 2001;311(1):173-182.

5Ren PH, Lauckner JE, Kachirskaia I, Heuser JE, Melki R, Kopito RR. Cytoplasmic penetration and persistent infection of mammalian cells by polyglutamine aggregates. Nat Cell Biol. Feb 2009;11(2):219-225.

6Chung W-S, Clarke LE, Wang GX, et al. Astrocytes mediate synapse elimination through MEGF10 and MERTK pathways. Nature. 11/24 2013;504(7480):394-400.

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    In December of 2017, Donald Trump made history by recognizing Jerusalem as the capital of Israel. Why is this big news? Because by this the Jewish people of Israel are now able to press forward in bringing about the Third Temple prophesied in the Bible.

    Jewish Rabbis have publicly announced that their Messiah will be revealed in the coming years who will be a leader and spiritual guide to all nations, gathering all religions under the worship of one God.

    Biblical prophecy tells us that this Jewish Messiah who will take the stage will be the antichrist “who opposes and exalts himself above all that is called God or that is worshiped, so that he sits as God in the temple of God, showing himself that he is God” (2 Thessalonians 2:4). For a time he will bring about a false peace, but “Therefore when you see the ‘abomination of desolation,’ spoken of by Daniel the prophet, standing in the holy place (Matthew 24:15)…then there will be great tribulation, such as has not been since the beginning of the world until this time, no, nor ever shall be” (Matthew 24:21).

    More importantly, the power that runs the world wants to put a RFID microchip in our body making us total slaves to them. This chip matches perfectly with the Mark of the Beast in the Bible, more specifically in Revelation 13:16-18:

    “He causes all, both small and great, rich and poor, free and slave, to receive a mark on their right hand or on their foreheads, and that no one may buy or sell except one who has the mark or the name of the beast, or the number of his name.

    Here is wisdom. Let him who has understanding calculate the number of the beast, for it is the number of a man: His number is 666.”

    Referring to the last days, this could only be speaking of a cashless society, which we have yet to see, but are heading towards. Otherwise, we could still buy or sell without the mark amongst others if physical money was still currency. This Mark couldn’t be spiritual because the word references two different physical locations. If it was spiritual it would just say in the forehead. RFID microchip implant technology will be the future of a one world cashless society containing digital currency. It will be implanted in the right-hand or the forehead, and we cannot buy or sell without it. Revelation 13:11-18 tells us that a false prophet will arise on the world scene doing miracles before men, deceiving them to receive this Mark. Do not be deceived! We must grow strong in Jesus. AT ALL COSTS, DO NOT TAKE IT!

    “Then a third angel followed them, saying with a loud voice, “If anyone worships the beast and his image, and receives his mark on his forehead or on his hand, he himself shall also drink of the wine of the wrath of God, which is poured out full strength into the cup of His indignation. He shall be tormented with fire and brimstone in the presence of the holy angels and in the presence of the Lamb. And the smoke of their torment ascends forever and ever; and they have no rest day or night, who worship the beast and his image, and whoever receives the mark of his name” (Revelation 14:9-11).

    People have been saying the end is coming for many years, but we needed two key things. One, the Third Temple, and two, the technology for a cashless society to fulfill the prophecy of the Mark of the Beast.

    Visit http://WWW.BIBLEFREEDOM.COM to see proof for these things and why the Bible truly is the word of God!

    If you haven’t already, it is time to seek God with all your heart. Jesus loves you more than you could imagine. He wants to have a relationship with you and redeem you from your sins. Turn to Him and repent while there is still hope! This is forever…God bless!

    “EITHER HUMAN INTELLIGENCE ULTIMATELY OWES ITS ORIGIN TO MINDLESS MATTER OR THERE IS A CREATOR…” – JOHN LENNOX

    We all know God exists. Why? Because without Him, we couldn’t prove anything at all. Do we live our lives as if we cannot know anything? No. So why is God necessary? In order to know anything for certain, you would have to know everything, or have revelation from somebody who does. Who is capable of knowing everything? God. So to know anything, you would have to be God, or know God.

    A worldview without God cannot account for the uniformity and intelligibility of nature. And why is it that we can even reason that God is the best explanation for this if there is no God? We are given reason to know or reject God, but never to know that He does not exist.

    It has been calculated by Roger Penrose that the odds of the initial conditions for the big bang to produce the universe that we see to be a number so big, that we could put a zero on every particle in the universe, and even that would not be enough to use every zero. What are the odds that God created the universe? Odds are no such thing. Who of you would gamble your life on one coin flip?

    Is there evidence that the Bible is the truth? Yes. Did you know that the creation accounts listed in the book of Genesis are not only all correct, but are also in the correct chronological order? That the Bible doesn’t say the Earth was formed in six 24-hour days but rather six long but finite periods of time? That the Bible makes 10 times more creation claims than all major “holy” books combined with no contradictions, while these other books have errors in them? The Bible stood alone by concurring with the big bang saying, “In the beginning God created the heaven and the earth” (Genesis 1:1); and says our universe is expanding, thousands of years before scientists discovered these things. Watch a potential life-changing video on the website listed below with Astronomer(PhD) Hugh Ross explaining all these facts based on published scientific data. He has authored many books, backed even by atheist scientists.

    Jesus came to pay a debt that we could not; to be our legal justifier to reconcile us back to a Holy God; only if we are willing to receive Him: “For the wages of sin is death…” (Romans 6:23).

    God so loved the world that He gave us His only begotten son, so that whoever believes in Him, through faith, shall not perish, but have everlasting life. Jesus says if we wish to enter into life to keep the commands! The two greatest commands are to love God with all your heart, soul, strength, and mind; and your neighbor as yourself. All the law hang on these commands. We must be born of and lead by the Holy Spirit, to be called children of God, to inherit the kingdom. If we are willing to humble ourselves in prayer to Jesus, to confess and forsake our sins, He is willing to give the Holy Spirit to those who keep asking of Him; giving us a new heart, leading us into all truth!

    Jesus came to free us from the bondage of sin. The everlasting fire was prepared for the devil and his angels due to disobedience to God’s law. If we do the same, what makes us any different than the devil? Jesus says unless we repent, we shall perish. For sin is the transgression of the law. We must walk in the Spirit so we may not fulfill the lusts of the flesh, being hatred, fornication, drunkenness and the like. Whoever practices such things will not inherit the kingdom (Galatians 5:16-26). If we sin, we may come before Jesus to ask for forgiveness (1 John 2:1-2). Evil thoughts are not sins, but rather temptations. It is not until these thoughts conceive and give birth by our own desires that they become sin (James 1:12-15). When we sin, we become in the likeness of the devil’s image, for he who sins is of the devil (1 John 3:8); but if we obey Jesus, in the image of God. For without holiness, we shall not see the Lord (Hebrews 12:14).

    The oldest religion in the world is holiness through faith (James 1:27). What religion did Adam and Eve follow before the fall? Jesus, Who became the last Adam, what religion does He follow? Is He not holy? He never told us to follow the rituals and traditions of man but to take up our cross and follow Him (Luke 9:23). There are many false doctrines being taught leading people astray. This is why we need the Holy Spirit for discernment. Unlike religion, holiness cannot be created. It is given to us from above by the baptism of the Spirit. Jesus is more than a religion; He is about having a personal relationship with the Father. Start by reading the Gospel of Matthew, to hear the words of God, to know His character and commandments. Follow and obey Jesus, for He is the way, the truth, and the life!

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