Molecular Motors. Structural and Mechanistic Overview! Kimberly Nguyen - December 6, 2013! MOLECULAR MOTORS - KIMBERLY NGUYEN
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1 Molecular Motors Structural and Mechanistic Overview!! Kimberly Nguyen - December 6, 2013!! 1
2 Molecular Motors: A Structure and Mechanism Overview! Introduction! Molecular motors are fundamental agents of movement within living organisms. Biological processes like muscle contraction, organelle migration, protein movement along DNA, rotation of bacterial flagellum, and synthesis of ATP are driven by molecular motors. Tension generated through muscle fibers allow the muscle to lengthen and shorten. Organelles can navigate the cytoskeleton to transport cargo throughout the cell. Specific proteins are responsible for the unpackaging of genes of the organism. Bacteria are able to propel themselves throughout their environment. And protons can traverse a gradient to propel the subunits of the ATP synthase, generating ATP (Garrett, 2013).! Clearly, molecular motors possess a fascinating ability to drive movement within living organisms. The question is, how do the structural components of motor proteins come together to drive movement within living organisms? This paper seeks to investigate the structural components of motor proteins and the conformational changes they take on to achieve biological movement within living organisms.! Molecular motors are spatially and temporally well-organized and perform directionally unified movements. The mechanisms that generate these unified movements are driven by two umbrella mechanisms: the linear walking mechanism and the rotary based propulsion mechanism. Linear motors walk along polymer lattice, while rotating motors turn protein subunits to induce propulsion. As will be discussed in this paper, myosin, kinesin, dynein, and the helicase utilize the linear walking movement, while bacterial flagella and the ATP synthase function through rotary-based propulsion (Garrett, 2013).!! Linear Walking Mechanisms! Cyclic conformational changes within the structure of motor proteins drive the walking mechanism of linear motors. Muscle contractions by myosin via the actin-myosin complex can be broken down into an arbitrary division of four steps. The organelle transport by kinesin and dynein into three and four steps, respectively; and unpackaging of DNA by helicase into five. All of these conformational changes are driven by energy from ATP.! Foremost, the structure of actin and myosin must be acknowledged in order to understand the mechanism behind muscle contraction. Cellular actin has two forms, the free standing monomeric globular form called the G-actin and the linear polymeric filamentous 2
3 form called F-actin. Microfilaments involved in muscle contraction consist of a double helix structure wound from two parallel F-actin strands (Dominguez, 2010). A diagram of both G- actin and F-actin is included and labeled Figure A (Actin, n.d.). The top half of the diagram depicts a simple model of free monomeric G-actin, while the bottom half of the diagram depicts a simply model of linear polymeric F-actin filaments (Actin, n.d.).! Figure A. Myosin, unlike actin, is possesses more varied components. Myosin is composed of a head, neck, and tail domain. The N-terminus is located at the start of the head and the C- terminus is located at the end of the tail. The head domain is composed of two heavy chains that form two globular heads. The heads each contain both an ATP binding site and an actin binding site. The neck domain links the head and tail domain and acts as a level for the conformational changes within myosin. The tail domain is composed of four light chains that form an alpha helix. The C-terminus at the end of the helix contains ionic bonds between myosin subunits, assisting in stabilization of the myosin backbone (Rayment, 1993). A diagram of a general myosin structure is included and labeled Figure B (Myosin Structure, n.d.). The left side depicts the tail and C-terminus, while the right side depicts the globular heads and N-terminus.! Figure B. 3
4 The actin-myosin complex is composed of myosin and actin arranged such that myosin filaments slide unidirectionally along bundles of F-actin filaments. In context of the sarcomere, which is the contractile unit of muscle cells, the myosin filaments are arranged in opposite directions, such that the myosin filaments cause the actin filaments to slide toward the middle of the sarcomere. The inward tension leads to contraction of the sarcomere without change in filament length. A diagram from MBInfo of the actin-myosin complex is included and labeled Figure C. The top half of the diagram depicts the sarcomere relaxed, while the bottom half depicts the sarcomere when contracted (List of figures, n.d.).! Figure C.! 4
5 To break down the steps, this explanation will begin by choosing an arbitrary starting point, when the myosin is bound to the actin filament. When the myosin is bound to the actin filament, the conformation of the myosin globular head is in a low energy conformation. The first step is the binding of ATP to the myosin head. ATP binding causes dissociation of the myosin from the actin. Come the addition of water, ATP is hydrolyzed, cleaving into ADP and Pi during step 2. During step 3, the hydrolysis induces a conformational change in the myosin head, bringing the myosin head back up toward the actin filament, forming a cross bridge. The subsequent release of ADP and Pi provides energy for the power stroke seen in step 4. The power stroke pulls on the actin filament in a unilateral direction. The cycle then ends after the power stroke and returns to the starting point, when the myosin head is back to its low energy conformation. A schematic diagram is included and labeled Figure D. (Molecular Mechanism of Force Generation in Biological Systems, n.d.).! Figure D. The overall structure of kinesin is remarkably similar to that of myosin. Like the head domain of myosin, the head domain of kinesin is composed of heavy chains that comprise its two globular heads at the amino terminal end. The globular heads each have two binding sites, one for the binding of ATP and the other for that of the microtubule on which the kinesin traverses. Kinesin likewise possesses a neck that links the head domain to the tail domain. The tail domain of kinesin is also composed of light chains that form an alpha helical 5
6 coil, which ends in a carboxyl terminal (Marx, 2009). A cartoon image of kinesin is included and labeled Figure E (News, n.d.).! Figure E. The mechanism of kinesin differs only slightly from that of myosin in the actin-myosin complex. The motility cycle of kinesin begins with each of the kinesin heads bound to the tubulin surface. The heads are connected to the coil by a neck linker segments. In the proceeding step, ATP binding induces a conformational change within the neck linkers, flipping the trailing head by 160 degrees, over and then beyond the leading head toward the next tubulin binding site. In step 3, the new leading head binds to a new site on the tubulin surface and releases ADP. During this time, the trailing head hydrolyzes ATP to ADP and Pi. In the final step 4 of the motility cycle, ATP binds to the leading head, and Pi dissociates from the trailing head (Marx, 2009). A schematic representation of the cyclic conformations is included and labeled Figure F. The mechanism proceeds from top to bottom, with the tag and colored feet of the kinesin to represent the movement of the hand-over-hand mechanism described (News, n.d.).! 6
7 ! The active movement of kinesins supports several cellular functions, including mitosis, meiosis, and transport of cellular cargo. Most kinesins walk toward the plus end of the microtubule, generally transporting cargo from the center of the cell toward the periphery. Dyneins, in contrast, are motor proteins that move toward the minus end. Dyneins are the next motor protein in discussion (Garrett, 2013).! Cytoplasmic dynein has two heavy chains with globular heads, each with their own stalk that walks along the microtubule. The heavy chains are connected to the light chains via a stem that shorten and elongate based on whether ADP is bound. The light chains link the stem to the cargo, enabling the dynein to transport its cargo (Robert, 2013).! Figure G.! The mechanism of dynein is essentially like that of kinesis. Dynein uses power strokes to walk hand-over-hand along the microtubule. First, ATP binds to the motor domain, promoting dissociation of dynein from the microtubule. Second, hydrolysis of ATP causes a conformational change that primes the structure for a power stroke. Third, microtubule movement is initiated by tight binding to the tip of the stalk. Fourth, the release of ADP and Pi from the catalytic site causes tilting of the stalk at the end of the cycle, pulling the dynein 7
8 and its cargo in the intended direction. A schematic representation is included and is labeled Figure G. The steps of the cyclic conformational changes involved in the hand-over-hand mechanism by dynein can be views in the direction of the arrows depicted (Robert, 2013).!! Dynein does differ starkly from kinesin in one fascinating way: while kinesin takes consistent and relatively linear steps, dynein takes much more irregular and directionally varied steps. According to a research team at Harvard, the dynein walk can be described as that of a drunken sailor. Research is still on-going (Cameron, 2012).!! The last of the linear motors in discussion is the helicase. In general, the helicase motors of superfamily 1 and 2 are monomers that consist of two reca domains in tandem repeat. Specifically, the Rep helicase from Escherichia Coli (E. Coli), the helicase that has been studied the most, exhibits the hand-over-hand mechanism that was discussed with dyneins. An image of a general helicase of the superfamily 1 and 2 is included and labeled Figure H. The domains are depicted in tandem (Garrett, 2013).!! Figure H.!! The helicase moves and unpackages DNA through three generally complex steps. Put simply, the first step can be described as beginning with the Rep dimer bound to ssdna. Second, the binding of ATP induces a conformational change that causes the on Rep monomer to bind to ssdna and the other to dsdna. Third, unwinding of dsdna and ATP hydrolysis occur. The unwound dsdna enable the binding of each Rep monomer to each of the current ssdna. Release of ADP and Pi causes Rep dimer to bind once again to ssdna, as was described in the initial step but this time further along the DNA substrate, completing the motility cycle. A schematic representation of the motility cycle is included and labeled Figure I. The mechanism proceeds to the right (Garrett, 2013).! 8
9 Figure I.! Rotary Propulsion Mechanisms!! Three protein motors have been unambiguously identified as rotary engines: the bacterial flagellar motor and the two motors that constitute ATP synthase (F0 and F1 ATPase). Of these, the bacterial flagellar motor and F0 motors derive their energy from ion-motive transmembrane force, while the F1 motor is driven by ATP hydrolysis, as like the linear motors discussed. Here, the paper reviews the current understanding of how these motor proteins convert their respective energy supply into rotary torque (Oster, 2003).!! Rotating motors consist of a rotating element, the rotor, and a stationary element, the stator. The bacterial flagellum rotating element comprises of three parts: a motor anchored in the bacterial inner membrane, a long filament that acts as the propellor, and a hook that works like a joint, connecting the motor to the filament. The bacterial flagellum stationary element is formed from the proteins mota and mot B, eight complexes of which surround the rotary motor (Oster, 2003). A computer generated image is included and labeled Figure J&K The left side is a three dimensional representation, whereas the right side is a twodimensional representation (Xing, 2006).!! Having considered the structure of the bacterial flagellar motor, it is time to review the transmembrane ion-motive force mentioned earlier that drives the rotary torque that steers the movement of bacteria. Gradients of protons and Na+ ions exist across bacterial inner membranes, typically with more H+ and Na+ ions outside of the cell. Regarding the wellstudied case of E. Coli, it is the spontaneous inward flow of protons through the mota-motb complexes that drive the rotation of the motor (Oxford Molecular Motors, n.d.).! 9
10 Figure J&K.! In a similar manner, the F0 and F1 motors of the ATP synthase perform rotary torque as well. Structurally, the ATP synthase is composed of two motors, the F0 and the F1. F0 is similar to the bacterial flagellar motor since it also uses transmembrane ion-motive force. F1, on the other hand, derives its energy from ATP hydrolysis, like the linear motor proteins discussed in the first half of the paper. The F1 unit has a stator and rotor that is formed from three hydrophobic subunits.there are six ATP-binding sites within the F1 structure, each arranged at the interface of adjacent subunits. Altogether, F0 acts as the transmembrane channel through which protons bind and move through to generate ATP from ADP and Pi (Garrett, 2013). A diagram is included and labeled Figure L. The figure separates out the F0 and F1 of the F0-F1 complex (Oster, 2003).! Figure L. 10
11 As a starting point, how does the cell obtain potential for the transmembrane ionmotive force in the first place? Within biological cells, there is an active transport of H+ to one side of a membrane, forming an electrical gradient. The gradient exists because there is one side in which more H+ exist, giving it a positive charge; meanwhile there is another side with less H+, lending it a negative charge. The H+, through laws of physics and chemistry, diffuse naturally across the membrane from areas of high concentration to areas of low concentration in order to create an equilibrium. The potential is made useful by, instead of letting the H+ diffuse passively on its own, the ATP synthase forms a channel that takes the energy from the gradient and makes it useful. This is transmembrane ion-motive force (Garrett, 2013).! The F0 rotary torque is generated via transmembrane ion-motive force. First, protons enter the inlet half-channel within the a subunit. From there, the protons are transferred to binding sites on the c subunits. The transfer and flow of protons through the F0 structure turns the rotor and generates a torque that drives the cyclic conformational changes that synthesize ATP (Garrett, 2013).!! Conclusion! As discussed, molecular motors are fundamental agents of movement within living organisms. Essential processes like muscle contraction, bidirectional migration of organelles within the cytoplasm, unpackaging of DNA by helicases, rotation of the bacterial flagellum and the synthesis of ATP are all driven by molecular motors.! The actin-myosin complex works through the friction between sliding thick and thin filaments. Tension generated through the friction allows for the muscle to lengthen and shorten. Kinesin and dynein bind and walk hand-over-hand along microtubules within the cell cytoplasm carrying cargo toward and away from the center of the cell. Specific proteins like helicases are responsible for the unpackaging of genes of an organism, and they can only achieve this by possessing the ability to traverse DNA. Bacteria are able to swim, propelling themselves throughout their environment as a result of an aggregate of transmembrane ionmotive force that drives the rotary torque of its flagella. And protons flowing through a gradient can induce the rotary torque needed to generate perhaps the most important component of all life, the ATP (Garrett, 2013).! From contraction to traveling, from propulsion to chemo-mechanical energy coupling, it is unequivocal that molecular motors play a fundamental role in all biological life forms. 11
12 References!!!!!!!!!! Actin. (n.d.). University of Illinois at Chicago. Retrieved December 6, 2013, from!! Cameron, D. (2012, January 8). HMS. Molecular Motor Struts Like Drunken Sailor. Retrieved! December 6, 2013, from Dominguez, R., & Holmes, K. C. (2010). Actin Structure And Function. Annual Review of!! Biophysics, 40(1), ! Garrett, R., & Grisham, C. M. (2013). Biochemistry (5th ed.). Belmont, CA: Brooks/Cole,!! Cengage Learning.! List of figures. (n.d.). MBInfo - A Modular Approach to Cellular Functions. Retrieved!! December 6, 2013, from Marx, A., Hoenger, A., & Mandelkow, E. (2009). Structures Of Kinesin Motor Proteins. Cell!! Motility and the Cytoskeleton, 66(11), ! Molecular Mechanism of Force Generation in Biological Systems. (n.d.). The University of! Rhode Island. Retrieved December 5, 2013, from forcegeneration.html! Myosin Structure. (n.d.). St. Steward's University. Retrieved December 6, 2013, from! STRUCT~1.HTM! News. (n.d.). Physics Illinois. Retrieved December 6, 2013, from!! Oxford Molecular Motors. (n.d.). Department of Physics. Retrieved December 6, 2013, from! Oster, G., & Wang, H. (2003). Rotary Protein Motors. Trends in Cell Biology, 13(3), ! Rayment, I., Holden, H., Whittaker, M., Yohn, C., Lorenz, M., Holmes, K., et al. (1993).!! Structure Of The Actin-myosin Complex And Its Implications For Muscle Contraction.!! Science, 261(5117), ! Roberts, A. (2013). Functions and mechanics of dynein motor proteins. Nature, 14, ! Xing, J. (2006). Torque-speed Relationship Of The Bacterial Flagellar Motor. Proceedings of!! the National Academy of Sciences, 103(5),
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